Roesel_online.pdf - Refubium

Aus dem Institut für Parasitologie und Tropenveterinärmedizin

des Fachbereichs Veterinärmedizin

der Freien Universität Berlin

und dem

International Livestock Research Institute

Assessment of the parasitic burden in the smallholder pig value chain

and implications for public health in Uganda

Inaugural-Dissertation

zur Erlangung des Grades eines

PhD of Biomedical Sciences

an der

Freien Universität Berlin

vorgelegt von

Kristina Rösel

Tierärztin

aus Karl-Marx-Stadt (jetzt Chemnitz)

Berlin 2017

Journal-Nr.: 3973

Gedruckt mit Genehmigung

des Fachbereichs Veterinärmedizin

der Freien Universität Berlin

Dekan: Univ.-Prof. Dr. Jürgen Zentek

Erster Gutachter: Prof. Dr. Peter-Henning Clausen

Zweiter Gutachter: Univ.-Prof. Dr. Reinhard Fries

Dritter Gutachter: Prof. Dr. Eric Fèvre

Deskriptoren (nach CAB-Thesaurus): pigs, value chain, animal parasitic nematodes, Trichinella

spp., muscle larvae, newborn larvae, Toxoplasma gondii, public health, epidemiology, meat

hygiene, animal housing, Uganda

Tag der Promotion: 30.11.2017

Coverbild: Angella Musewa/ILRI

“Overcoming poverty is not a task of charity, it is an act of justice.” (Nelson Mandela)

Dedicated to the smallholder pig value chain actors in Uganda.

Table of contents

i

TABLE OF CONTENTS

List of figures ................................................................................................................................. iii

List of tables .................................................................................................................................... v

List of abbreviations ...................................................................................................................... vi

1 Preface ..................................................................................................................................... 1

1.1 Introduction and study objectives ..................................................................................... 1

1.2 Structure of the thesis ....................................................................................................... 3

2 Literature review ...................................................................................................................... 4

2.1 The history of pigs in Africa ............................................................................................. 4

2.2 Smallholder pig production systems in sub-Saharan Africa ............................................. 6

2.3 Parasites of domestic pigs and their occurrence in East Africa ...................................... 12

2.3.1 Trematoda (flukes) .......................................................................................................... 12

2.3.2 Nematoda (roundworms) ................................................................................................ 12

2.3.3 Protozoa .......................................................................................................................... 17

3 The context for researching smallholder pig value chains in Uganda ................................... 20

3.1 CGIAR Research Framework ......................................................................................... 20

3.2 Study area ....................................................................................................................... 22

3.3 Study site selection and characteristics........................................................................... 25

3.3.1 Geographical targeting .................................................................................................... 25

3.3.2 Stakeholder consultation ................................................................................................. 25

4 Parasites as a production constraint in smallholder pig production systems

(Publications I & II) ............................................................................................................... 28

5 Parasites with potential implications for public health (Publications III & IV) .................... 54

6 Knowledge, attitudes and practices of pork consumers (Publication V) ............................... 72

7 Summarizing discussion ........................................................................................................ 79

7.1 Value chain domains as a suitable proxy for the classification of heterogeneous

smallholder pig production systems ............................................................................... 79

7.2 Pig parasites as a constraint to farm productivity ........................................................... 80

7.3 Parasite infections with public health implications ........................................................ 81

7.3.1 Gastrointestinal parasites as soil-transmitted zoonotic helminths .................................. 81

7.3.2 Pork-borne zoonoses ....................................................................................................... 81

Table of contents

ii

7.4 Researching smallholder pig value chains through an integrated approach and

participatory methods ..................................................................................................... 85

7.5 Concluding remarks, limitations of the survey and potential future research ................ 87

7.5.1 Major research findings .................................................................................................. 87

7.5.2 Major conclusions ........................................................................................................... 88

8 References .............................................................................................................................. 91

Summary ..................................................................................................................................... 108

Zusammenfassung....................................................................................................................... 110

List of own publications.............................................................................................................. 112

Disclosure of own share in the body of the work ....................................................................... 124

Acknowledgements ..................................................................................................................... 126

Statement of authorship .............................................................................................................. 128

List of figures

iii

List of figures

Figure 2.1 Tethered local breed in Wakiso district, Central Uganda (Kristina Roesel). ................ 5

Figure 2.2 Exotic breed (Large White) in a commercial farm in Masaka district,

Central Uganda (Kristina Roesel). ............................................................................... 5

Figure 2.3 Fully confined cross-breed pig in an intensive production unit in Wakiso district,


Figure 2.4 Ugandan pig farmer tends to her Camborough pigs

(Edgar R. Batte in Uganda Daily Monitor, 7 November 2012 (Muhanguzi, 2012)). .. 5

Figure 2.5 Pig tethered under a tree and provided with sweet potato vines for feed,

Kiboga district in Central Uganda (Kristina Roesel). .................................................. 8

Figure 2.6 Adult pig confined but piglets able to roam freely in Kamuli district,

Eastern Uganda (Kristina Roesel). ............................................................................... 8

Figure 2.7 One type of confinement in a rural setting in peri-urban Wakiso district,


Figure 2.8 Pigs confined in Kamuli district, Eastern Uganda (Kristina Roesel). ........................... 8

Figure 2.9 Confined pigs in peri-urban Masaka, Masaka district, Central Uganda

(Kristina Roesel). ......................................................................................................... 8

Figure 2.10 Commercial pig farm with biosecurity protocol in peri-urban Kampala

(Kristina Roesel) .......................................................................................................... 8

Figure 2.11 The distribution of encapsulated Trichinella spp. in Africa reviewed by

Mukaratirwa et al. (2013), Murrell and Pozio (2011), Pozio (2007), and

Pozio et al. (2005). Map adapted from Pozio et al. (2005). ....................................... 16

Figure 3.1 A livestock value chain and its actors and beneficiaries.

Source: Nick Taylor, University of Reading, and Jonathan Rushton,

Royal Veterinary College, In: Roesel and Grace (2014). .......................................... 20

Figure 3.2 Delivering CGIAR Research Program on Livestock & Fish (CRP L&F).

Structure: Three integrated components. Source: CRP L&F, 2012. .......................... 21

Figure 3.3 Problem tree showing food safety and related market access in the context of

whole value chain development (ILRI, 2011). .......................................................... 22

Figure 3.4 Pig density by district shows a higher concentration in the Central, Western and

Eastern regions of Uganda. Source: Poole et al. (2015).

Category thresholds are as accurate as 14 decimals. ................................................. 23

Figure 3.5 Average pig densities in Uganda show production specific production foci in Mbale,

peri-urban Kampala, Kasese and Masaka. Source: Robinson et al. (2014).

Category thresholds are as accurate as 14 decimals. ................................................. 24

List of figures

iv

Figure 3.6 Spatial distribution of per capita pig meat consumption, based on population density.

Source: Center for International Earth Science Information

Network (CIESIN), 2011. Category thresholds are as accurate as 14 decimals. ....... 24

Figure 3.7 The CRP L&F study sites selected in 2012: Masaka and Mukono districts in the

Central region; Kamuli district in the Eastern region of Uganda

(ILRI/Pamela Ochungo). ............................................................................................ 26

Figure 7.1 An article published by the newspaper Uganda Daily Monitor on 6 June 2012

referring to a report that suggests high contamination of pork in Kampala.

On inquiry, the Kampala City Council Authority's (KCCA) senior veterinary

officer explained that there is no report. Statements on pork safety were

based on misperceptions not evidence.

Source: Safe Food, Fair Food blog post (ILRI, 2012c). ............................................ 84

Figure 7.2 One week later, on 13 June 2016, the Ugandan populist newspaper

Red Pepper declared a war on informal pork butcheries operating in Kampala,

referring to the same misleading “expert report”.

Source: Safe Food, Fair Food blog post (ILRI, 2012c). ............................................ 84

Figure 7.3 Synthesized results of the Ugandan smallholder pig value chain assessment

including porcine parasites. The work was presented by the author at

Tropentag conference in Prague, September 2014. Source: Ouma et al. (2014). ...... 86

List of tables

v

List of tables

Table 2.1 Simplified and selective classification of pig endoparasites.

Adapted from Deplazes et al. (2016), Gajadhar (2015), Greve (2012),

Lindsay et al. (2012), Kaufmann (1996). ....................................................................... 9

Table 2.2 Common ectoparasites of domestic pigs and their relevance

to the pig farm enterprise and public health.

Adapted from Deplazes et al. (2016) and Greve and Davies (2012). .......................... 11

Table 3.1 The final sites selected for the pig value chain assessment under the CRP L&F.

Source: Poole et al. (2015). .......................................................................................... 26

Table 3.2 Characteristics of the sites selected by the CRP L&F.

Sources: MAAIF/UBOS (2009); Twinomujini et al. (2011). ...................................... 27

Table 7.1 The median global numbers of foodborne illnesses, deaths and Disability Adjusted

Life Years (DALYs) compared to the median rates of DALYs

in the African sub-region E (AFR E) which includes Uganda.

Source: Havelaar et al. (2015). ..................................................................................... 83

List of abbreviations

vi


AIDS Acquired immunodeficiency syndrome

AAT Animal African trypanosomosis

ADG Average daily (weight) gain

ASF African swine fever

BMZ Bundesministerium für wirtschaftliche Zusammenarbeit und Entwicklung

(German Federal Ministry for Economic Cooperation and Development)

CGIAR Global research partnership for a food-secure future (formerly Consultative

Group for International Agricultural Research)

CI Confidence interval

CIESIN Center for International Earth Science Information Network

CRP CGIAR Research Program

CRP A4NH CGIAR Research Program on Agriculture for Nutrition and Health

CRP L&F CGIAR Research Program on Livestock and Fish

CSF Classical swine fever

DAD-IS Domestic Animal Diversity Information System

DALYs Disability Adjusted Life Years

ELISA Enzyme-linked immunosorbent assay

FAO Food and Agricultural Organization of the United Nations

FAOSTAT Statistics Division of the Food and Agricultural Organization of the United

Nations

FGD Focus group discussion

FMD Foot and mouth disease

GIS Geographic information system

GIZ Gesellschaft für Internationale Zusammenarbeit

HAT Human African trypanosomosis

HIV Human immunodeficiency virus

IFAD International Fund for Agricultural Development

IgG Immunoglobulin G

ILRI International Livestock Research Institute

IFPRI International Food Policy Research Institute


vii

KCCA Kampala City Council Authority

LC Local government council

MAAIF Ministry of Agriculture, Animal Industry and Fisheries (Government of Uganda)

NAADS National Agricultural Advisory Service

NEMA National Environment Management Agency

NGO Non-governmental organization

OIE World Organization for Animal Health

PCV Porcine circovirus

PE Participatory epidemiology

PRA Participatory rural appraisal

PRRS Porcine Reproductive and Respiratory Syndrome

RR Rural production for rural consumption (value chain type)

RU Rural production for urban consumption (value chain type)

SFFF Safe Food, Fair Food project

SPVCD Smallholder Pig Value Chain Development project

STH Soil-transmitted helminths

UBOS Uganda Bureau of Statistics

UU Urban production for urban consumption (value chain type)

VEDCO Volunteer Efforts for Development Concerns

WHO World Health Organization

Chapter 1: Preface

1 Preface

1.1 Introduction and study objectives

Population growth, urbanization and increasing consumers’ demand for products of animal origin

are fuelling the so-called Livestock Revolution which could provide poor smallholder farmers with

income (Delgado et al., 2001; Thornton, 2010) and thus contribute to poverty alleviation. In low-

income countries, meat and dairy consumption have grown at average annual rates of 5.1 and

3.6%, respectively, between 1971 and 2007 (Alexandratos and Bruinsma, 2012). Between 2000

and 2050, demand for livestock products is estimated to nearly double in sub-Saharan Africa

(Thornton, 2010), while globally, potential improvements in food security and nutrition could

benefit directly more than 750 million poor livestock keepers (Food and Agriculture Organization

of the United Nations (FAO), 2011). Uganda’s population is currently growing at 3.3% annually

(Worldbank, 2015a), and has increased seven times since the 1950s. The country is experiencing

rapid urbanization – like most developing countries – at currently 4.5% which could result in an

increase in the population of Uganda's cities from 6.4 million today to more than 30 million within

the next two decades (Worldbank, 2015b), demanding ever more food.

Pork is the most popular meat in the world today accounting for over 36% of the world meat

production, followed by poultry and beef (FAO, 2015). In Uganda, pork has only become

important over the past 25 years; the Statistics Division of the Food and Agricultural Organization

of the United Nations (FAOSTAT) estimated pig numbers have grown rapidly from 716,400 in

1989 to 2.18 million in 2008 (FAOSTAT, 2016). The 2008 national livestock census recorded 3.2

million pigs (Ministry of Agriculture, Animal Industry and Fisheries (MAAIF)/ Uganda Bureau

of Statistics (UBOS), 2009), significantly surpassing estimates of the FAO. Whereas pork

accounted for barely 1% of the annual per capita meat consumption in Uganda in 1961, it made up

27% of all meat consumed in 2011 (FAOSTAT, 2011). Little information is available regarding

the structure and composition of the pig sector in Uganda but it has been documented that almost

one fifth of the Ugandan households own pigs, on average three (MAAIF/ UBOS, 2009), while up

to 70% of all pork consumed in Uganda is consumed in urban and peri-urban areas (International

Livestock Research Institute (ILRI), 2011).

The majority of pigs in Kenya, Tanzania and Uganda are estimated to be reared in smallholder

households under extensive systems (Lekule and Kyvsgaard, 2003); e.g. mostly free-ranging with

tethering. Conventional knowledge states that traditional production systems are wasteful and

unprofitable due to poor feed conversion, low reproductive rates, final products of inferior quality,

and losses due to high animal mortality. A high gastrointestinal parasitic burden and direct losses

due to infectious animal diseases such as African swine fever, foot and mouth disease or rabies

(all endemic in Uganda) could contribute to low productivity (World Organisation for Animal

Health (OIE), 2016). Concurrent with growth in smallholder pig keeping and pork consumption,

zoonoses such as mycobacterial infections and porcine cysticercosis have increasingly been

reported (Muwonge et al., 2010; Waiswa et al., 2009; Phiri et al., 2003). However, traditional

production also has advantages compared to intensive systems, for example the small inputs

required in traditional production (little to no housing), and the pig’s natural scavenging behaviour

which allows them to feed on kitchen waste and agricultural waste that would otherwise be wasted.

The surging demand for livestock products provides an opportunity to set poor farmers on

pathways out of poverty by increasing production outputs and market access. At the same time,

1

Chapter 1: Preface

markets have become more demanding and threaten the continued presence of smallholder

farmers: livestock diseases and other factors affect a constant supply while foodborne pathogens

may impair the quality and safety of the farmers’ products. While the presence of food safety

hazards such as bacteria, parasites or drug residues in informally marketed food is high, the risk to

human health is mostly unknown and current food safety management is both ineffective and

inequitable.

In Uganda, intensification level may affect the parasitic burden of pigs and hence the profitability

of pig farming as well as the risk to human health associated with pork borne parasites. The present

study aimed to contribute to improving selected smallholder pig value chains in Uganda by

increasing the knowledge on prevalent parasitic diseases.

Specific objectives are to:

1. understand whether parasites are perceived as a production constraint by farmers;

2. estimate the burden of selected endoparasites in pigs and pork at farm, slaughter and retail

outlet level in three selected value chain types in Uganda. These parasites included

common gastrointestinal helminths and protozoa, as well as two major porkborne zoonotic

parasites Trichinella spp. and Toxoplasma gondii;

3. identify risk factors contributing to parasitic infections in pigs and pork, in order to better

understand the epidemiology of parasitic diseases in these value chains with emphasis on

pork borne zoonoses;

4. identify current practices that increase or reduce risks to public health associated with pork

consumption;

5. assess the risk to public health through the consumption of pork infested with parasites.

2

Chapter 1: Preface

1.2 Structure of the thesis

This cumulative thesis is structured as follows:

Chapter 1 Preface: introduction, study objectives and structure of the thesis.

Chapter 2 Literature review: outlines the history of pigs in Africa, describes the current

smallholder pig production systems in sub-Saharan Africa, and reviews the current state of

knowledge on parasitic pig diseases compromising farm productivity as well as selected parasitic

diseases that are potentially transmitted to humans through pork consumption. The review refers

to previous research from sub-Saharan Africa, and particularly Uganda.

Chapter 3 Research context: describes the context of the study and how it fits into overarching

research for development on smallholder pig value chains in Uganda. It further describes how

study sites were selected, value chain systems defined and characteristics of the area under study.

Chapter 4 Parasites as a production constraint: shows that gastrointestinal parasites are

perceived as an important production constraint by smallholder pig farmers in Central and Eastern

Uganda (Publication I) and summarizes baseline information on the prevalence and risk factors of

the most common intestinal parasites (Publication II).

Chapter 5 Parasites with implications for public health: provides baseline information on two

pork borne zoonoses of global importance, namely infection with Trichinella spp. (Publication III)

and Toxoplasma gondii (Publication IV), in smallholder pig value chains in Central and Eastern

Uganda.

Chapter 6 Knowledge, attitudes and practices of pork consumers: outlines the findings on

common preparation and consumption practices as well as sources of pork for consumption in the

study area to potentially draw conclusions on the risk to pork consumers (Publication V).

Chapter 7 Summarizing discussion: discusses major findings, conclusions and limitations of

the study, and generates assumptions for potential interventions and further research.

3

Chapter 2: Literature review

2 Literature review

2.1 The history of pigs in Africa

Literature on the domestication of pigs in Africa is scarce and highly debated (Amills et al., 2013;

Blench, 2000). The domestic pig (Sus scrofa domesticus) was domesticated from its ancestor the

wild boar, or Eurasian wild pig (Sus scrofa) which is a native to Europe, Asia and North Africa.

There are three distinct wild members of the family Suidae in tropical Africa: the bushpig

(Potamochoerus porcus), the warthog (Phacochoerus aethiopicus), and the giant forest hog

(Hylochoerus meinertzhageni). It is still debated to what extent African wild Suidae were

domesticated (Gifford-Gonzalez and Hanotte, 2011; Blench, 2000; Haltenorth and Diller, 1980);

but evidence is appearing that bush pigs and domestic pigs have indeed mated (Rothschild et al.,

2014).

Genetic and archaeological findings suggest that pig domestication began about 9,000 to 10,000

years ago at multiple sites across Eurasia, followed by their subsequent worldwide spread through

increased exploration and commercialization (Amills et al., 2010; Larson, 2005). According to

recent findings (Amills et al., 2013; Ramirez et al., 2009; Blench, 2000), it is likely that domestic

pigs have been introduced to sub-Saharan Africa from the Near East via Egypt approximately

6,000 years ago, from the Far East during the Indian Ocean trade in the 7th century, and during

European colonisation from the 15th century. By analysing the genetic diversity of African pigs,

Ramirez et al. (2009) showed the existence of a clear genetic dichotomy between East and West

Africa: While a clear Far Eastern genetic signature was found in pigs from the Indian Ocean coast

of Africa, it could not be detected in pigs from the African Atlantic shores. The findings have been

discussed in-depth (Gifford-Gonzalez and Hanotte, 2011; Ramirez et al., 2009). It has also been

hypothesized that African pig breeds were domesticated locally and independently in the Nile

Delta (Gautier, 2002; Houlihan, 1997); however, at present evidence is still weak (Amills et al.,

2013). African pig breeds are still poorly characterised but according to the Domestic Animal

Diversity Information System (DAD-IS) database hosted by FAO, there are currently 148 pig

breeds in Africa (FAO, 2016).

Phenotypically, domestic pigs in Uganda are divided into two major groups, the so-called “local”

pigs and the introduced “exotic” pigs. Local pigs are usually black with medium-sized, semi-erect

ears, a straight tail and a long snout (Figure 2.1). Exotic breeds such as Large White (Figure 2.2),

Landrace and Saddleback have been introduced during the colonial periods. Under local

management practices, local and exotic breeds interbred (Figure 2.3). Other pig breeds such as

Camborough® have recently become of interest to Ugandan pig keepers (Muhanguzi, 2012). The

Camborough® (Figure 2.4) is a product (material pig line) of a South Africa-based franchise of a

commercial pig breeding company called the Pig Improvement Company (PIC

International)1. The breed is derived from original crosses followed by heavy selection for

maternal traits. Approximately 40 Camborough® lines have been released by PIC over the past

years, and some have been introduced to Uganda by the Ministry of Agriculture (personal

communication).

The distribution of religion in Africa is another critical aspect of the history of pigs in Africa

(Blench, 2000). Muslims and Ethiopian Christian Orthodox are forbidden to eat pork which is

generally interpreted as a prohibition on any sort of contact with pigs. Islam spread to Africa in

1 http://www.picgenus.com/

4

http://www.picgenus.com/


the early 7th century when Muslims sought refuge in present-day Ethiopia during the Migration to

Abyssinia (hijarat); in Uganda, they arrived only in the late 19th century (David, 2004). Until the

spread of Islam, pigs were quite important, especially in the Egyptian and Berber cultures in

Northern Africa, already 6,000 years ago (Blench, 2000). All aspects of pig-keeping have been

relatively little researched in Africa. Even international research organizations – such as ILRI since

its inception in 1974 – have not included pigs in Africa in its research agenda until recently. Blench

(2000) argues this may have been related to prejudice against pigs from potential donor agencies

but also the belief that – as monogastric animals – pigs may compete with humans for food.

Figure 2.1 Tethered local breed in Wakiso district, Central

Uganda (Kristina Roesel).

Figure 2.2 Exotic breed (Large White) in a commercial farm

in Masaka district, Central Uganda (Kristina Roesel).

Figure 2.3 Fully confined cross-breed pig in an intensive

production unit in Wakiso district, Central Uganda (Kristina

Roesel).

Figure 2.4 Ugandan pig farmer tends to her Camborough

pigs (Edgar R. Batte in Uganda Daily Monitor, 7 November

2012 (Muhanguzi, 2012)).

5

2.2 Smallholder pig production systems in sub-Saharan Africa

Pig production has emerged as an important agribusiness over the past few decades. Not only in

Uganda but in many regions of sub-Saharan Africa, e.g. Nigeria (Machebe et al., 2009;

Adesehinwa et al., 2003), Ethiopia (Tekle et al., 2013; Seid and Abebaw, 2010), Tanzania

(Karimuribo et al., 2011; Esrony et al., 1997), Namibia (Petrus et al., 2011) and Kenya (Obonyo

et al., 2013; Kagira et al., 2010b; Mutua et al., 2010; Wabacha et al., 2004a) to mention but a few.

Given population growth and the pressure on the size of farm land, monogastrics seem to provide

better production efficiency per unit area of land (FAO, 2009; Wabacha et al., 2004a). In Western

Kenya, for instance, the average size of a smallholder pig farmers’ land is one acre2 or less (Mutua

et al., 2011a; Kagira et al., 2010b). Pigs are often reared by women (Obonyo et al., 2013; Petrus

et al., 2011; Kagira et al., 2010b; Mutua et al., 2010; Nsoso et al., 2006) as one of several income-

generating activities, and kept in close proximity to homesteads (Obonyo et al., 2013; Karimuribo

et al., 2011; Mutua et al., 2010). Income generation as well as savings and insurance against family

emergency is often a more important motivation for pig keeping than providing meat for house

hold consumption (Mbuthia et al., 2015; Tekle et al., 2013; Mutua et al., 2010). The regular

smallholder in Kenya and Uganda keeps 3-5 pigs (Kagira et al., 2010b; MAAIF/UBOS, 2009);

and herd size increases with proximity to urban centres (MAAIF/UBOS, 2009), with the level of

intensification (Mbuthia et al., 2015; Wabacha et al., 2004a), or concentrates in certain areas; this

is the case in Ethiopia where pig keeping is increasing but not as commonly practiced due stringent

religious laws (Tekle et al., 2013). Most of the pig farmers in traditional production systems in

sub-Saharan Africa keep cross-breeds (Kagira et al., 2010b) as they believe local breeds require

less feeds and are more tolerant to diseases (Petrus et al., 2011; Lekule and Kyvsgaard, 2003) while

exotic breeds grow faster.

Many small-scale farmers sell live animals produced in farrow-to-weaner (piglet) and porker-to-

finisher (fattening) units; few keep boars and those who do often rent them out to other farmers

for breeding (Muhanguzi et al., 2012; Kagira et al., 2010b), often against in-kind payment with a

piglet. Many of the pigs are kept in mixed confinement systems, often tethered, especially during

crop season, and otherwise free-roaming, especially during dry seasons when crop fields are

fallowing and feeds are scarce (Obonyo et al., 2013; Mutua et al., 2011a; Permin et al., 1999).

Housing is difficult to provide for many farmers because it is considered too expensive, and shelter

is often just temporary or rarely cleaned (Muhanguzi et al., 2012; Kagira et al., 2010b; Seid and

Abebaw, 2010). A study in rural Western Kenya reported that if farmers did not consider housing

unnecessary altogether, the main reasons for non-confinement are fear of the pig damaging the

houses, lack of food to provide for confined pigs, houses becoming muddy during the rainy season

and farmers lacking the time to manage confined pigs (Mutua et al., 2011a). Smallholders’ pigs

are mostly fed with locally available ingredients such as crop residues (Muhanguzi et al., 2012;

Kagira et al., 2010b; Petrus et al., 2011) but in some areas pigs are left grazing/scavenging or fed

with household leftovers (Obonyo et al., 2013; Seid and Abebaw, 2010), supplemented with

commercial feeds such as sunflower seed cake (Karimuribo et al., 2011), wheat bran (Tekle et al.,

2013), or ruminal contents from abattoirs (Muhanguzi et al., 2012). Marketing is often

disorganised and economically inefficient because record keeping is not common (Nsoso et al.,

2006; Wabacha et al., 2004a); farmers mostly sell when they are in need (e.g. for school fees), and

they do not weigh their animals and have therefore no objective basis for negotiation (Mutua et

2 one acre equals approx. 4,000 square metres

6


al., 2011a, 2011b; Petrus et al., 2011). Many other knowledge gaps on pig husbandry such as how

to feed monogastrics, regular provision of water and the difference between treatment and

vaccination have been documented in Kenya, and some of them seem to depend on the presence

and a positive attitude towards pig-keeping of the veterinary extension service in a region (Obonyo

et al., 2013; Mutua et al., 2011a; Kagira et al., 2010b).

Pig diseases (especially African swine fever and parasitic infestation), cost of feeds, lack of market

access and veterinary extension as well as lack of knowledge on pig husbandry and disease

prevention are perceived to be the greatest production constraints in many pig-keeping

communities in sub-Saharan Africa (Atuhaire et al., 2013; Tekle et al., 2013; Muhanguzi et al.,

2012; Karimuribo et al., 2011; Petrus et al., 2011; Kagira et al., 2010b). Important parasitic

diseases (based on signs observed by farmers) are sarcoptic mange, lice and gastrointestinal worms

(Karimuribo et al., 2011; Petrus et al., 2011; Kagira et al., 2010b). Different pig production systems

in Uganda are illustrated in Figures 2.5-2.10.

7


Figure 2.5 Pig tethered under a tree and provided with sweet

potato vines for feed, Kiboga district in Central Uganda

(Kristina Roesel).

Figure 2.6 Adult pig confined but piglets able to roam freely

in Kamuli district, Eastern Uganda (Kristina Roesel).

Figure 2.7 One type of confinement in a rural setting in peri-

urban Wakiso district, Central Uganda (Kristina Roesel).

Figure 2.8 Pigs confined in Kamuli district, Eastern Uganda

(Kristina Roesel).

Figure 2.9 Confined pigs in peri-urban Masaka, Masaka

district, Central Uganda (Kristina Roesel).

Figure 2.10 Commercial pig farm with biosecurity protocol

in peri-urban Kampala (Kristina Roesel).

8


Table 2.1 Simplified and selective classification of pig endoparasites. Adapted from Deplazes et al. (2016), Gajadhar (2015), Greve (2012), Lindsay et al. (2012), Kaufmann

(1996).

Order: species Common name Location in the pig host Economic relevance Zoonotic relevance

Cest

od

a

Cyclophyllidea: Taenia solium,

larval

Pork tapeworm,

pork measles

Muscle tissue At slaughter if infected meat is

condemned.

Ingestion of Cysticercus cellulosae in pork causes

taeniosis in humans; infection in pigs helps maintaining the life cycle. High risk for humans developing

neurocysticercosis when ingesting T. solium eggs

(autoinfection).

Cyclophyllidea: Taenia

hydatigena, larval

Omentum, mesentery Losses through trimming at slaughter. N/A

Cyclophyllidea: Echinococcus granulosus s.l., larval

Hydatid disease Liver, lungs At slaughter if infected organs are condemned.

Pigs can be a reservoir for echinococcosis in carnivores (maintain life cycle). Humans are accidental hosts when

ingesting eggs of E. intermedius (pig strain G7) passed in

dog faeces.

Trem

ato

da

3

Echinostomida: Fasciola

hepatica

Liver fluke Liver (bile system) At slaughter if infected livers are

condemned.

Accidental infection of humans through ingestion of

encysted metacercaria.

Strigeatida: Alaria alata Muscle tissue At slaughter if infected meat is condemned.

Emerging parasitic disease. Human infection through ingestion of mesocercaria.

Plagiorchiida: Paragonimus spp. Lungs N/A N/A

Nem

ato

da

4

Ascarida: Ascaris suum Large intestinal

roundworm

Lumen of small intestine Major growth reduction if piglets are

infected.

Especially for children in poor pig-keeping communities.

Enoplidae: Trichuris suis Whipworm Large intestine Haemorrhagic enteritis in heavy infection; weight losses in chronic infections.

Potential still under debate.

Rhabditida: Strongyloides suis

(syn. ransomi)

Threadworm Epithelium small intestine Major impact in suckling piglets. Larva migrans cutanea (creeping eruption).

Strongylida: Hyostrongylus

rubidus

Red stomach

worm

Stomach fundus Suck small amounts of blood and cause

catarrhal gastritis.

N/A

Strongylida: Metastrongylus apri Lung worm Bronchial tubes and

bronchioles

Respiratory disease, especially in young

pigs; can facilitate infection with

pathogens causing pneumonia.

N/A

Strongylida: Oesophagostomum

spp.

Nodular worm Large intestine Reoccuring enteritis with every new

infection (no protective immunity).

N/A

Strongylida: Globocephalus spp. Pig hookworm Attached to mucosa of

small intestine.

Aenemia in growers. N/A

Strongylida: Ollulanus tricuspis Stomach Weight loss and chronic-catarrhal gastritis. N/A

Strongylida: Stephanurus dentatus

Swine kidney worm

Peri-renal fat tissue Reduced growth; trimming at slaughter due to abscesses.

N/A

3 less significant trematodes reported in pigs: Dicrocoelium hospes, Gastrodiscus aegyptiacus, Postharmostomum suis, Schistosoma bovis, Schistosoma matthei, Eurytrema pancreaticum, Gongylonema pulchrum, Prosthogonimus cuneatus 4 less significant nematodes reported in pigs: Gongylonema pulchrum, Setaria congolensis, Gnathosoma hispidum, Trichostrongylus axei

9


Table 2.1 (continued). Simplified and selective classification of pig endoparasites. Adapted from Deplazes et al. (2016), Gajadhar (2015), Greve (2012), Lindsay et al. (2012),

Kaufmann (1996).

Order: species Common name Location in the pig host Economic relevance Zoonotic relevance

Nem

ato

da

4

Oligacanthorhynchida:

Macracanthorhynchus hirudinaceus

Thorny-headed

worms

Attached to mucosa of

small intestine

Only if burden is high. Accidental infection through ingestion of infected

arthropod.

Sprirurida:

Physocephalus sexalatus; Ascarops strongylina;

Gnathosoma spinigerum;

Simondsia paradoxa

Thick stomach

worms

Stomach Less important than H. rubidus. N/A

Spirurida: Gongylonema pulchrum

Esophageal worm Epithelium of tongue and esophagus

Minor irritation. Humans are susceptible but must ingest intermediate host insect to become infected.

Trichocephalida: Trichinella spp. Pork worm,

muscle worm

Adults in epithelium of

small intestines; first-stage

larvae encysted in striated muscle.

Not in pig farms but potentially at

slaughter if infected carcasses are

condemned.

Human trichinellosis mostly caused by ingestion of viable

first-stage larvae in infected and undercooked pork.

Pro

tozo

a5

Cryptosporida: Cryptosporidium

spp.

Epithelium of small

intestine

Diarrhoea in growers. C. parvum and C. suis are human-infective.

Eimeriida: Eimeria spp.

Epithelium of small intestine

Diarrhoea in weaners and finishers. N/A

Eimeriida:

Isospora suis

Epithelium of small

intestine

Diarrhoea in piglets. N/A

Eimeriida:

Toxoplasma gondii

Muscle and brain tissue Not in pig farms but potentially at

slaughter if infected carcasses are

condemned.

Undercooked pork considered source of foodborne

infection; occupational exposure to infective bradyzoites.

Eimeriida: Sarcocystis spp.

Muscle tissue On farm piglet diarrhoea. Transient diarrhoea in humans.

Eimeriida:

Neospora caninum

Nervous tissue On farm piglet losses due to abortions and

stillbirth.

N/A

Piroplasmida: Babesia trautmanni

Porcine piroplasmosis

Erythrocytes Up to 50% mortality in infected pigs of all ages.

N/A

Trypanosomatida: Trypanosoma spp.

Nagana Extracellular blood Peracute death in pigs caused by T. simiae or T. suis; reservoir for cattle pathogenic

trypanosomes.

Pigs as reservoir for human pathogenic Trypanosoma spp.

Diplomonadida:

Giardia duodenalis6

Small intestine Subclinical Assemblages A and B causative agent of human

giardiasis.

Vestibuliferida: Balantidium coli Large intestine Haemorrhagic enteritis if burden is high. Faecal-oral transmission route; low pathogenicity but

discussed as contributing factor to colitis.

4 less significant nematodes reported in pigs: Gongylonema pulchrum, Setaria congolensis, Gnathosoma hispidum, Trichostrongylus axei 5 less significant protozoa reported in pigs: Tritrichomonas suis, Trichomonas rotunda, Tetratrichomonas buttreyi, Entamoeba suis (syn. polecki) 6 syn. lamblia, syn. intestinales

10


Table 2.2 Common ectoparasites of domestic pigs and their relevance to the pig farm enterprise and public health. Adapted from Deplazes et al. (2016) and Greve and Davies

(2012).

Order: species Common name Economic relevance Zoonotic relevance

Art

hro

pod

a

Astigmata: Sarcoptes scabiei var. suis Sarcoptic mange mite, burrowing mite

Reduction of growth rates, feed efficiency, and fertility.

Transient and self-limiting dermatitis in humans.

Prostigmata: Demodex phylloides (syn. suis) Follicular mange mite, follicle mite N/A N/A

Metastigmata: Ornithodorus moubata complex Soft tick (e.g. eyeless tampan) Vector for African swine fever virus. Vector for rickettsiosis.

Metastigmata: Amblyomma/ Rhipicephalus spp. Hard tick (e.g. bont/blue/brown tick) Nuisance and hence stress-induced reduced growth rate or anaemia; vector for porcine

babesiosis

N/A

Phthiraptera: Haematopinus suis Hog louse, sucking louse Reduced growth and increased susceptibility to

disease in piglets due to anaemia; discussed as vector for African swine fever virus.

N/A

Siphonaptera: Tunga penetrans Sand flea, jigger flea Nuisance Pigs as reservoir for human tungiasis.

Siphonaptera: Pulex irritans/ Ctenocephalides

felis/ Echidnophaga gallinaecea

Human flea/ cat flea/ sticktight flea Nuisance N/A

Diptera: Musca domestica House fly Nuisance Mechanical vector of pathogens (faecal-oral

route).

Diptera: Stomoxys calcitrans Stable fly Nuisance and potential vector of pig pathogens N/A

Diptera: Chrysomyia bezziana, Calliphora spp. etc.

Screwworm/ blow fly/ carrion fly/ flesh fly

Excavation of primary wounds (myiasis, or fly strike) and exposure to secondary infections

N/A

Diptera: Glossina spp. Tsetse fly Vector for nagana in pigs caused by T. simiae or

T. suis; vector for cattle pathogenic Trypanosoma spp.

Vector for human pathogenic Trypanosoma

species for which pigs can be reservoirs.

Diptera: Aedes spp./ Culex spp. Mosquito Mechanical vector for PRRS virus and Mycoplasma (Eperythropozoon) suis.

Potential vector for human pathogenic arboviruses (e.g. Japanese encephalitis, West Nile fever,

Tahyna).

Diptera: Phlebotomus spp. Sand fly N/A N/A

Diptera: Simulium spp. Black fly/ gnat Nuisance N/A

Diptera: Culicoides spp. Biting midge Nuisance N/A

11


2.3 Parasites of domestic pigs and their occurrence in East Africa

In general, pig parasites can be divided into two major groups: endo- and ectoparasites.

Endoparasites live within the host, either inside the gastrointestinal lumen or organ tissue such as

liver, lungs or muscle. Many of them are heteroxenous, an important trait that needs to be

considered in diagnostics, management and control. This group of endoparasites in pigs (Table

2.1) includes representatives of major economic importance and the potential to cause disease in

humans. Ectoparasites (Table 2.2) are usually found outside of the pig’s body, on or in the skin,

either temporary or permanently. Many of them are economically important as a nuisance and as

a consequence, decreased weight gain due to the animals’ pressure to deter them. Others are known

vectors for more debilitating diseases, including parasites, such as ticks transmitting the African

swine fever virus or tsetse flies carrying Trypanosoma species. The following section outlines the

biology and occurrence of the endoparasites economic and veterinary public health importance

that are subject to this study, with particular reference to East Africa and Uganda. For the

denomination of parasitic diseases or infections, the author followed the Standardized

Nomenclature of Animal Parasitic Diseases (Kassai et al., 1988).

2.3.1 Trematoda (flukes)

Fasciola (F.) hepatica and Fasciola (F.) gigantica, the common or gigantic liver flukes, are

trematodes with a broad range of mammal hosts including ruminants, horses, camels, pigs and

humans. Pigs are not very susceptible to infection with Fasciola but can be carriers of adult flukes

shedding eggs (very rare). The World Health Organization (WHO) estimates that at least 2.4

million people are infected in more than 70 countries worldwide with several million at risk; and

that no continent is free from fasciolosis, and it is likely that where animal cases are reported,

human cases also exist (WHO, 2016a). In livestock production, the burden is mainly on herbivores,

especially ruminants (sheep > goat > cattle), and the result of reduced growth performance,

anaemia and condemnation of infected livers if meat inspection takes place and condemnation is

enforced. In Kenya, liver condemnation at beef cattle abattoirs due to fasciolosis led to losses

worth $25,000 in 2007 and 2008 (Kanyari et al., 2012). The life cycle is indirect whereby the pigs

ingest encysted metacercaria with contaminated food (pasture) or water. Within one day, juvenile

flukes penetrate the intestinal wall and migrate to the liver where they migrate the tissue for about

six weeks, and then move through the bile system. This can take months to years; from there up to

20,000 eggs per female per day are produced 8 to 10 weeks post infection at the earliest. The eggs

are passed in the pig faeces and develop in water where a miracidium hatches and penetrates

freshwater molluscs (Galba trunculata or Lymnaea natalensis) where it produces hundreds of

cercariae. These encyst on plants where they develop into infective metacercaria. They can survive

up to 10 weeks in a moist environment such as wetlands. In Uganda F. gigantica has been reported

in bovines from Mt. Elgon (Howell et al., 2012); and both F. gigantica and F. hepatica were

reported from the tropical highlands in Tanzania (Walker et al., 2008). Kagira et al. (2012) reported

3% of the pigs in Western Kenya infected with Fasciola spp. using McMaster fecal flotation

technique.

2.3.2 Nematoda (roundworms)

Ascaris (A.) suum, the large roundworm of the small intestine, is cosmopolitan in domestic and

wild Suidae. Infection is particularly important in the pig industry for two reasons: first, the adult

worms compete with their pig host for nutrients through disruption of enteral absorption which

12


reduces feed efficiency and average daily gains (Hale et al., 1985); secondly, once on the pig farm,

it is difficult to control because the eggs are extremely resilient and difficult to eliminate.

Reproduction follows a direct life cycle: ingestion of the egg with infectious third-stage larvae,

which hatches in the lumen of the jejunum and penetrates the intestinal wall, then migrates into

the liver via the portal vena where it migrates the tissue for one to two days causing temporary

inflammation and the well-known milk spots which disappear again after about 25 days once larval

burden decreases. Within the next week larvae are carried to the lungs where migration causes

inflammation and, potentially, respiratory signs. In the lungs larvae moult and further move to the

bronchioles from where they are coughed up and swallowed. About two weeks post infection the

larvae reach the small intestine again where they mature into adults. After another 4-6 weeks

females start laying eggs, sometimes more than 200,000 per day for about six months. The un-

embryonated eggs have a thick shell, which enables them to survive in moist soil for up to five

years. Most chemicals do not have an effect on the egg and they have a sticky coat which enables

them to be easily carried from farm to farm by live vectors (i.e. flies, beetles, cats or dogs but also

children) or other vectors (i.e. boots, vehicles, tools). Also, they can stick to the sow’s coat from

where nursing piglets ingest the eggs when suckling. Infection and clinical signs occur mostly in

pigs younger than five months, with age there is increased immunity though adult pigs may still

harbour worms that produce eggs intermittently. A. suum can infect humans, and recent research

including the application of molecular diagnostics increasingly suggests the possibility that A.

lumbricoides may be closely related or even be the same species as A. suum (Iñiguez et al., 2012;

Leles et al., 2012; Liu et al., 2012; Peng and Criscione, 2012; Zhou et al., 2012).

Trichuris (Tr.) suis, due to its whip-like oesophagus, is commonly known as the whipworm and

primarily located in the large intestine where it permanently penetrates the epithelium. This causes

minimal lesions which are consider to offer an entry point for swine dysentery complex (Beer,

1973; Greve, 2012); heavy infections are associated with haemorrhagic enteritis while chronic

infection may cause reduced growth. In experiments, pigs infected with Tr. suis required up to

33% more feeds (Hale and Stewart, 1979). Reproduction follows a direct life cycle, whereby the

egg with an infectious first-stage larvae is ingested and penetrates the walls of the smaller intestine

and caecum. Four moults inside the wall follow over the next two weeks and six to seven weeks

post infection, eggs are shed intermittently over the five month life span of the adult worm (Beer,

1973). It takes the first-stage larvae two months to reach infectivity which makes herd infection

better manageable. However, the eggs can remain viable on the ground for many years. The results

of genetic analysis of Trichuris species (Tr. suis and Tr. trichuria) obtained from naturally infected

pigs and humans in Uganda suggest cross-infections of humans with Tr. suis (Nissen et al., 2012).

Strongyloides (S.) ransomi is a very small threadworm (3-5 mm) that is found worldwide but

especially in the tropical and subtropical areas where temperature and humidity are favourable.

This roundworm is particularly pathogenic in nursing piglets (within first 10-14 days) and causes

poor weight gains (stunting) due to the destruction of the small intestines’ epithelium where the

adult worms are located. Malabsorption, diarrhoea, dullness, hypo-albuminaemia, and alterations

of organs (i.e. skin, liver, kidney, spleen, urinary bladder etc.) and even death may occur if the

burden is high. Reproduction follows a direct life cycle, and infection of the pig host with third-

stage larvae occur most often either orally through ingestion or by skin penetration. Through

penetration of the buccal mucosa or thin skin (i.e. hoof skin, belly) they reach the lymph vessels

and migrate to the heart and lungs from where they are coughed up and swallowed (tracheal

migration). By the time they reach the small intestines (6 to 10 days), they have developed into

13


parthogenic adult females laying embryonated eggs within a shell (up to 2,000 per day) that appear

in the faeces. The larvae hatch within a few hours, and develop into an infective third-stage larvae

within 3 to 4 days (and 2 moults). Besides that homogonic cycle, some of the larvae develop into

free-living males and females who sexually produce infective larvae after a few generations

(heterogonic cycle). A less common but potential infection of nursing piglets occurs via colostrum

as infective larvae can accumulate in the sow’s mammary fat for over 2.5. years; in the piglet,

larvae develop directly into adult worms causing diarrhoea only a few days after infection.

Acquired immunity is strong and therefore, older pigs are not usually presenting with clinical signs

in case of infection.

Hyostrongylus (H.) rubidus (red stomach worm) is a nematode specific to swine (Deplazes et al.,

2016) whose adults are found lodged in the stomach where they suck small amounts of blood. At

higher burdens infection causes catarrhal gastritis and eventually, the potential erosion of the

gastric mucosa may cause significant weight losses (Stewart et al., 1985) as well as anaemia, lack

of milk and fertility problems. Reproduction of the roundworm follows a direct life cycle, whereby

the pig ingests the infective third-stage larvae which moults twice in the stomach’s fundus glands

and matures into adults. The first eggs with the characteristic strongyle morula appear in the faeces

after 16 to 22 days. Within one week, a first-stage larvae has developed inside the egg, hatches

and migrates from the faeces onto the grass from where it moults twice into infectious third-stage

larvae and is eventually ingested by pigs feeding on pasture. In older animals, hypobiosis is

possible after the first moult in the stomach fundus glands and they are potentially reactivated

under peripartum stress.

Lung worms of porcines, the collective term for members of the genus Metastrongylus include

Metastrongylus (M.) apri, M. pudendotectus, and M. salmi in pigs, and mixed infections are

common. The adult worms (approx. 50 mm) are found in the pigs´ bronchi and bronchioli, live for

six to nine months and reproduce via indirect life cycle: the pigs ingest the infective third-stage

larvae lodged in earthworms on pasture. Within the pig, larvae penetrate the intestinal wall and

migrate through the lymph vessels to the right heart and lungs. Four to five weeks post infection,

adults have developed and start producing eggs which are coughed up, swallowed and then passed

in the faeces. They are thick-shelled with a rough coat and carry the embryonated first-stage larvae.

Earthworms ingest them and the larvae hatch and moult within the intermediate host. After about

ten days, the larvae in the earth worm has become infective for the pig. Clinical signs are only

found in heavy infection but lung tissue may be compromised due to the larval migration and

leaves the pig susceptible to secondary infection, e.g. Mycoplasma hyopneumoniae which then

presents with coughing. In young pigs up to six months, clinical signs such as coughing, bronchitis,

running nose, emphysema, anorexia and weight loss are more common; piglet mortality and

stunting may be high (Deplazes et al., 2016; Greve, 2012). Prevalence rates vary across East Africa

and are reported later in this section.

Two Oesophagostomum (Oe.) spp., Oe. dentatum and Oe. quadrispinulatum, are found in pigs

worldwide. All ages can be affected, but higher prevalence is usually found in older pigs where

the worms accumulate with age due to lacking acquired immunity. Infection causes enteritis that

may worsen with every new infection. The life cycle is direct: third-stage larvae are ingested by

the pig and enter the mucosal glands of the large intestine where they undergo moulting in the

lamina propria over the next two weeks causing the worm that gives rise to the common name of

the worm (nodular worm). The adults persist in the lumen of the large intestine for up to six

14


months, eggs are shed three to six weeks post infection. Once excreted, the third-stage larvae

develops in the faeces within one week and eventually, it moves away from the faeces onto the

grass from where it is ingested by a pasture-fed animal. Infection with Oesophagostomum spp. is

reported to extend the excretion of Salmonella Typhimurium in case of co-infection (Steenhard et

al., 2002).

In East African pigs, infection with gastrointestinal helminths has been frequently reported over

the past few years. Studies in Kenyan extensive and semi-intensive pig farms show that infection

with strongyles dominate, and where larvae were cultured Oesophagostomum spp. are the most

common followed by H. rubidus and a small fraction of Trichostrongylus spp. Infections with S.

ransomi are common, too, while eggs of Ascaris spp., Trichuris spp., Metastrongylus spp. and

spiruid eggs are found at varying levels (Obonyo et al., 2013; Kagira et al., 2012; Nganga et al.,

2008). The same studies reported that mixed infections are very common but findings on risk

factors diverged, especially with regards to the association between gastrointestinal worm

prevalence and deworming history (incl. frequency), housing and type of feeds. Interestingly, in

commercial farms in Central Kenya which supply formal pork processors and have a median of

60 animals, 94% of farms also showed infections with Oesophagostomum spp., A. suum, T. suis

and S. ransomi despite 48% reporting to regularly treat their animals with dewormers as well as

routine dung removal and disinfection (Kagira et al., 2008). In Tanzania, overall prevalences over

50% have been reported but infection with Oesophagostomum spp., A. suum, S. ransomi, and T.

suis were documented (Esrony et al., 1997), and significantly higher egg counts were found in

tropical highlands compared to the semi-arid zones. In Ethiopia, at least 25% of extensively

managed pigs were infected with at least one species of gastrointestinal helminth: A. suum (25.9%),

F. hepatica (1.8%), and T. suis (0.3%); moreover, 1.7% of the pigs carried oocysts of Eimeria spp.

and 7% of Cryptosporidium spp., and 72% of the soil samples in the study sites were contaminated

with A. suum eggs (Tomass et al., 2013). In growing pigs in Western Uganda, 89% of the animals

showed strongyle infections, 40% infection with A. suum, 17% with T. suis, and 48% spiruroid

eggs (Nissen et al., 2011). In the Eastern parts of the country, in Kamuli and Iganga districts, 94.8%

were infected, mainly with strongyles (55.2%), Metastrongylus spp. (49%), Coccidia oocysts

(68.6%), Ascaris spp. (42.2%), hookworms (18.6%), and Trichuris spp. (6.2%); 80.3 had mixed

infections (Waiswa et al., 2007). Other helminths of the gastrointestinal system are less common

and less pathogenic, except when burdens are very heavy (Table 2.1).

The nematode genus Trichinella is found everywhere except the Antarctica and comprises eight

species and four genotypes: five have been reported from Africa. Figure 2.11 shows the

distribution based on recent reviews (Mukaratirwa et al., 2013; Murrell and Pozio, 2011; Pozio,

2007; Pozio et al., 2005). While a wide range of host species can be infected (mammals, birds and

reptiles), only humans show clinical signs (Gottstein et al., 2009); infection is strictly related to

the consumption of raw or undercooked infected meat (Pozio, 2007). The life cycle is direct and

starts with the ingestion of infectious first-stage larvae in infected muscle tissue. Within the pig,

the larvae develop into adults (1-4 mm) within two days and lodge in the villi of the small

intestine’s epithelium. Females give birth to larvae in the lamina propria five days after mating

which may cause subclinical enteritis. The larvae are then carried away in the blood stream into

skeletal muscle cells which they transform into a nurse cell and where they mature into infective

and encysted first-stage larvae within two weeks. If the larvae do not enter muscle cells but other

organ tissue, they die in granulomas. The encysted muscle larvae is very resilient and survives

many years, even if the cyst starts calcifying or the infected carcass starts decaying. Transmission

15


to pigs can occur in case of tail biting within an infected herd, scavenging carcasses of wild,

infected animals (i.e. rodents) as well as feeding on garbage or kitchen swill that contains infected

meat scraps. Humans get infected in the same way, by ingesting infectious first-stage larvae in raw

or undercooked meat. The infection dose depends on the Trichinella species. Trichinella (T.)

spiralis is the most important and most researched Trichinella species in veterinary public health

and the ingestion of 500 first-stage larvae may result in diarrhoea, vomiting, high fever as well as

headache and periorbal oedema. At two to three weeks after infection muscle pain occurs and death

may result from cardiomyopathy and paralysis of respiratory muscles.

In 1962, Kozar presented a detailed and up-to-date account of the known distribution of

Trichinella. At that time, apart from the Mediterranean region, the map of Africa was a complete

blank (Nelson, 1970). Two years later, several outbreaks of the disease in humans in Kenya lead

to the discovery of an enzoonotic sylvatic cycle (Nelson, 1970), and since then wild animals have

increasingly been reported to carry Trichinella in Africa (Figure 2.11) (La Grange et al., 2013,

2010, 2009; Marucci et al., 2009; Pozio et al., 2007, 1997). Human outbreaks date back several

decades and were documented in Egypt (Sayed et al., 2010), Northwest Ethiopia (Kefenie and

Bero, 1992; Kefenie et al., 1988), Kenya (Kaminsky and Zimmerman, 1977) and Tanzania (Bura

and Willett, 1977). Studies on domestic pigs are rare but increasing: Trichinella-specific antibodies

have been found in 11-40% of surveyed pigs in Nigeria (Adediran et al., 2015; Momoh et al.,

2013) and in 0.8% of a study cohort of pigs in Madagascar (Rakotoharinome et al., 2014). Attempts

to isolate muscle larvae in pig abattoirs were unsuccessful in Tanzania and Ghana (Ngowi et al.,

2004; Permin et al., 1999) but T. spiralis has been isolated by means of artificial digestion from

domestic pigs in Egypt (Sayed et al., 2010; Morsy et al., 2000).

Figure 2.11 The distribution of Trichinella spp. in Africa reviewed by Mukaratirwa et al. (2013), Murrell and Pozio (2011), Pozio

(2007), and Pozio et al. (2005). Map adapted from Pozio et al. (2005).

16


2.3.3 Protozoa

Coccidia are very host specific protozoa, and pigs are susceptible to (mixed) infection with

Eimeria and Isospora (Levine and Ivens, 1986). Infection with Eimeria is usually considered

subclinical; however, while experimental infection with E. debliecki did not cause clinical disease

in suckling pigs or growers (Lindsay et al., 1987), infection with E. spinosa has indeed been

reported to cause clinical disease in weaners and finishers (Lindsay et al., 2002; Yaeger et al.,

2003). Infection with Isospora (I.) suis on the other hand can cause serious diarrhoea in nursing

piglets (piglet coccidiosis) and is of much higher significance to the pig industry. I. suis is found

globally, but mostly where pigs are kept in confinement. Infected suckling piglets appear healthy

until they suddenly develop a yellowish-grayish diarrhoea (caused by a catarrhal-necrotizing

enteritis), most often between the first and second week postpartum; morbidity in the litter is high,

and mortality moderate but it can increase rapidly with concurrent bacterial, viral or parasitic

infections (Lindsay et al., 2012). Piglets one to two days old at infection develop much more severe

disease than if infected at two to four weeks of age (Koudela and Kučerová, 1999). After pigs

ingest sporulated oocysts from their environment, they are excysted when passing the stomach and

small intestines. Here, the sporozoites are activated, leave the sporocyst and penetrate the

enterocytes. Endogenous development through asexual and sexual reproduction follows in the

cytoplasm of the enterocytes of the small intestine. Five days post infection, pigs pass un-

sporulated oocysts with their faeces; these are not yet infectious but sporogony into

environmentally very resistant oocysts follows rapidly after, if ambient temperature ranges

between 20-37°C (Lindsay et al., 1982). Pigs develop partial immunity but small amounts of

oocysts can be shed intermittently, and colostral antibodies do not prevent clinical coccidiosis in

piglets. Studies have shown that sows are apparently not the source of infection for suckling pigs

but that improved sanitation (including regular cleaning, disinfection, restricted farm access, pets

not entering farm, rodent control, sanitizing after every farrowing) has been the most successful

method for reducing losses due to piglet coccidiosis (Lindsay et al., 2012). In Eastern Uganda,

68.6% of the pigs have been found to pass coccidia oocysts (Waiswa et al., 2007); however,

oocysts were not sporulated and the prevalence was determined at animal level, not herd level.

Much lower levels of coccidia oocysts have been reported from Ethiopia (Tomass et al., 2013) and

infection with Eimeria spp. has been recorded in 33% of pigs studied in Western Kenya (Kagira

et al., 2010a).

Balantidium spp. is found in pigs and humans worldwide, but more commonly in tropical and

subtropical regions (Thompson and Smith, 2011). It has direct life cycle similar to Giardia, except

that infection is usually located in the large intestine. Infection in pigs and humans is usually

subclinical, but it is discussed as a contributing factor to colitis. Infection in pigs increases with

age but has not been found in pigs younger than four weeks (Schuster and Ramirez-Avila, 2008).

If the burden is high, then haemorrhagic enteritis may occur as the protozoa invade mucosal tissue.

Higher infection rates are sometimes associated with extensive pig keeping (reviewed by Schuster

and Ramirez-Avila, 2008) but the extent of this is not yet known. In West Africa, B. coli has been

found in pigs (Yatswako et al., 2007; Permin et al., 1999), raw vegetables (Ogbolu et al., 2009)

and non-human primates. In Western Kenya, 64% of pigs in extensive systems have been found

infected with B. coli (Kagira et al., 2010a).

Toxoplasmosis is a major zoonosis with a global distribution; it is caused by Toxoplasma (T.)

gondii. Infection is common where susceptible hosts have access to food, water, or soil

17


contaminated with sporulated oocysts passed in cat faeces. The life cycle is indirect with pigs as

intermediate host: pigs pick up sporulated oocysts from cat faeces or bradyzoites from infected

carcasses in the environment when scavenging. The oocysts survive passage through the stomach

and invade the lamina propria of the small intestine where they transform into quickly multiplying

tachyzoites. From there spread into the body through the blood stream and form cysts in brain and

muscle tissue for which they have a particular tropism. However, they can be found in virtually all

organ tissue. When forming tissue cysts, tachyzoites turn into bradyzoites that keep multiplying,

perhaps for the whole life of a food animal, but very slowly. If infected tissue of the intermediate

host is ingested by the definitive feline host, asexual and sexual multiplication takes place in the

cat’s intestines from where oocysts are shed into the environment again. These oocysts sporulate

within five days and can persist in moist and cool soil for up to one year. Tissue cysts have been

shown to be viable for up to 2.5 years and can be rendered nonviable by freezing at -12°C for three

days (Dubey, 1988) or salting/curing meat (Hill et al., 2004). Clinical toxoplasmosis is rare in pigs

(Dubey, 2009, 1986), but reproductive signs can occur such as abortion, stillbirth and foetal

mummification in females infected for the first time during gestation (Feitosa et al., 2014);

surviving piglets may be uncoordinated and show signs of tremor and coughing (Lindsay et al.,

2012). However, this is highly unlikely in settings where extensive production systems dominate.

Postnatal infection is more likely and may occur due to the ingestion of large numbers of oocysts,

e.g. in pig feeds, and clinical signs may include anorexia, fever, dyspnoea, limb weakness and even

death (Dubey, 2009; Weissenböck and Dubey, 1993). The presence of infected cats, rodents, or

birds is suggested to be the main source of infection for pigs; and herd size (e.g. risk for

cannibalism), source of water, disposal of dead pigs on the farm, garbage or swill feeding, cats

used for rodent control in pig feed stock have been reported to be risk factors (Feitosa et al., 2014;

Dubey, 2009; Weigel et al., 1995). Experimental studies also showed that dogs can be mechanical

vector of oocysts but sporulation does not occur in dog fur (Frenkel et al., 2003). Attempts to

develop pig vaccines are underway (Garcia, 2009).

Most human infections are asymptomatic in otherwise healthy people; approximately 25-30% of

the world’s human population is infected (Montoya and Liesenfeld, 2004) varying in geographical

regions, also depending on dietary habits, and increasing in resource-poor communities with

limited access to safe water (Bahia-Oliveira et al., 2003). The severity of toxoplasmosis depends

on the infection dose (Dubey, 1986) and the virulence of the genotype. A recent review by Robert-

Gangeux and Dardé (2012), found that in Africa the predominant genotypes are I and III

(cosmopolitan), coexisting with the Africa haplogroups 1 to 3. The synthesis of data in the review

also showed a higher rate of retinochoroiditis in Africa than in Europe. In Kampala, Uganda, all

three lineages have been reported in HIV-patients but also in chickens (Lindström et al., 2008,

2006) as well as one recombinant isolate of type II/III (Bontell et al., 2009).

Recent advances in molecular epidemiology suggest that there are no species-specific strains of T.

gondii, and that pigs can be infected with at least nine different genotypes (reviewed by Dubey,

2009). Nevertheless, studies on the prevalence of T. gondii infection in pigs in Africa is still

limited. In Nigeria, ELISA-based prevalences ranged from 25% on farms to 45.2% in slaughtered

pigs (Ayinmode and Abiola, 2016; Ayinmode and Olaosebikan, 2013) and 19.8% in dogs, which

are often used for food (Ayinmode et al., 2015). In Malagasy pigs, a seroprevalence of 22.8% was

reported (Rakotoharinome et al., 2014) while in Ghana 40.6% of 641 pigs were ELISA-positive

(Arko-Mensah et al., 2000), and in Ethiopian pigs the proportion was 32.1% (Gebremedhin et al.,

2015). Serological surveys in Zimbabwe showed that 9.3-26.8% of domestic pigs were ELISA-

18


positive, and IgGs have also been reported from wildlife and small ruminants (Hove, 2005; Hove

et al., 2005; Hove and Dubey, 1999); mouse-pathogenic T. gondii was isolated from a slaughtered

pig in Zimbabwe (Hove and Mukaratirwa, 2002). In Uganda, there is only one study on T. gondii

infection in livestock. It has investigated the IgG prevalence in goats and found 31% of the 784

animals originating from all parts of the country sero-positive; herd prevalence was 100% and

infection rates were significantly higher in urban locations (Bisson et al., 2000). Another sero-

survey on dogs kept near conservation areas showed very high levels of infection with T. gondii

and other, potentially zoonotic, agents (Millán et al., 2013).

In high-risk groups in the human population, namely sero-negative pregnant women or HIV-

patients, infection with any strain may result in severe clinical disease including foetal death

(abortion), congenital toxoplasmosis, encephalitis, or retinochoroiditis (Montoya and Liesenfeld,

2004). An estimated 50% of human toxoplasmosis can be attributed to foodborne transmission

where consumers ingest viable bradyzoites from raw or undercooked meat (Torgerson et al., 2014).

Estimates of the global burden have been limited to congenital toxoplasmosis for which the burden

is high at 1.2 million DALYs (Torgerson and Mastroiacovo, 2013). T. gondii is considered an

opportunistic pathogen and suggested to cause meningitis in HIV/Aids patients (Wright and Ford,

1995). A post mortem survey in Côte d’Ivoire showed cerebral toxoplasmosis in 21% of Aids

patients (Lucas et al., 1993). A previously subclinical infection can be reactivated and become

clinical if people’s immune system is supressed at a later time in life (Robert-Gangneux and Dardé,

2012), for instance through a disease or medication. Reactivation results from the rupture of tissue

cysts, a continuing process that is considered responsible for the continuous immune response in

a competent healthy human, which ensures dynamic control of the infection (Robert-Gangneux

and Dardé, 2012). Apart from the above-mentioned infection routes, people working with infected

meat have also been shown to be at higher risk to infection (Jones et al., 2009); potentially due to

accidentally ingesting bradyzoites from tissue cysts ruptured during slaughter or processing.

19


Chapter 3: Research context

3 The context for researching smallholder pig value chains in Uganda

Value chains resemble intricate webs and include all the links that start with the idea for a product

and continue through to the consumption of the product, often beyond to the disposal of the product

itself and its remainders. In the case of food products of animal origin, value chains include farm-

level inputs and services that enable its production (e.g. feeds, breeding services, animal health

services), transporting, processing, marketing and consumption of animal sourced foods and

related products (Figure 3.1). Moreover, value chains include institutional and governance

arrangements that facilitate the operation of these systems (e.g. Animal Disease or Meat Acts).

Value chain analysis considers how and by whom the value is utilized. Past livestock research in

low-income countries has focused on specific aspects of value chains, for instance on increased

farm output (e.g. by implementing interventions that reduce livestock disease burden but which

usually come at additional cost to the farmer) without considering if markets and purchasing power

are readily available.

Figure 3.1 A livestock value chain and its actors and beneficiaries. Source: Nick Taylor, University of Reading, and Jonathan

Rushton, Royal Veterinary College, In: Roesel and Grace (2014).

3.1 CGIAR Research Framework

In January 2012, the CGIAR launched research programs (CRP), in which different CGIAR

centres work in multi-centre and multi-disciplinary teams to increase research impact. The CRP

20


on Livestock and Fish (L&F), led by ILRI, has the overall goal to sustainably increase the

productivity of small-scale livestock and fish systems in order to make animal sourced foods more

available and more affordable for poor consumers, and in doing so, to reduce poverty and poverty-

related impact through greater participation (ILRI, 2012a).

Figure 3.2 Delivering CGIAR Research Program on Livestock & Fish (CRP L&F). Structure: Three integrated components. Source:

CRP L&F, 2012.

The program follows an integrated approach (Figure 3.2) to transform selected value chains in

targeted livestock and fish commodities in nine countries, one of them being the smallholder pig

value chain in Uganda. In 2012/13, as an initial step, the value chain was described, its actors and

products mapped and constraints and opportunities for growth of the pig sector in Uganda assessed.

In 2013/14, in-depth surveys quantified disease prevalence and other elements previously

established as important constraints. The results and implications have been discussed with

stakeholders and potential solutions to constraints tested in pilot studies from 2014 until today.

ILRI is also leading one of four components in the first phase of the CRP on Agriculture for

Nutrition and Health (A4NH), led by the International Food Policy Research Institute (IFPRI). The

rationale for this program is based on the assumption that agriculture provides poor people with

nutritious food and income from agricultural products (IFPRI, 2012). However, agricultural

activities, especially in livestock production, bear potential health risks. The Food Safety and

Zoonoses program of ILRI leads an A4NH research component on the prevention and control of

agriculture-associated diseases which has four major research areas: emerging infectious diseases,

food safety, neglected zoonoses, and One Health/Ecohealth (ILRI, 2012b).

The thesis presented here was aligned with both of the programs outlined above and part of the

research project Safe Food, Fair Food: Risk-based approaches to improving food safety and

market access in smallholder meat, milk and fish value chains in four African countries under

A4NH (ILRI, 2012c). The project’s overall aim is to generate evidence on risks from animal

sourced food products of which the majority in sub-Saharan Africa is sold in informal markets.

Figure 3.3 outlines why food safety should be one of the components considered in a livestock

value chain analysis and why this research was aligned with L&F.

21

Figure 3.3 Problem tree showing food safety and related market access in the context of whole value chain development (ILRI,

2011).

3.2 Study area

Uganda is located in Equatorial Africa, west of Kenya, south of South Sudan, east of the

Democratic Republic of the Congo and north of Tanzania and Rwanda. It is situated in the heart

of the Great Lakes region and much of its borders being freshwater lakeshore; however, Uganda

is landlocked with no access to the sea. The country covers a total surface area of 241,551 square

kilometres of which about 17.3% are open water and wetlands (National Environment

Management Agency (NEMA), 2009). Uganda’s climate is tropical but mostly temperate due to

its location on the African Plateau with average altitudes between 900 and 1,500 metres above sea

level (NEMA, 2009). While the semiarid north-eastern part of the country is characterized by an

intense hot and dry season (November to March) followed by a single rainy season from April to

August, the Central and southern parts of the country have seasonal rains with peaks in April/May

and October/November but rainfall of lower intensity throughout the year (NEMA, 2009). Given

the favourable climatic conditions, mixed crop-livestock systems are most common and covering

just over 75.0% of the land (Robinson et al., 2011), 14% is under grasslands supporting agro-

pastoral livestock production in the North-eastern part of the country, and mixed irrigated systems

do not cover even one percent of the surface land area.

Uganda has one of the youngest and most rapidly growing populations in the world; from 2011 to

2015, it increased by 13.1% from 34.5 million to 39.05 million (Worldbank, 2016). For

comparison, in 1991 the population counted 16.7 million (Twinomujini et al., 2011). More than

50% are younger than 15 years, well above sub-Sahara Africa’s average of 43.2%, and about

22


500,000 people are expected to enter the labour market every year (Worldbank, 2015c). Despite

good economic progress over the past few decades, about 62.0% and 78.5% of the population still

live on less than US$ 1.25 and US$ 2 per day, respectively (Center for International Earth Science

Information Network (CIESIN), 2011; Wood et al., 2010). Since 1993, when the Ugandan

Parliament enacted the Local Governments Statute, functions, powers and services were gradually

transferred from the central government to local governments (local government councils, LC).

By 2011, there were 112 districts spread across four administrative regions: Northern, Eastern,

Central and Western. Each district (LC5) is further divided into countries (LC4), sub-counties

(LC3), parishes (LC2) and zones/villages (LC1).

Figure 3.4 Pig density by district shows a higher concentration in the Central, Western and Eastern regions of Uganda. Source:

Poole et al. (2015). Category thresholds are as accurate as 14 decimals.

23


Pig keeping is practiced across the whole country with concentrations around Kampala, in the

Central and Western regions and to the east in the Soroti-Mbale area (Figures 3.4 and 3.5). Per

capita consumption of pig meat is 3.4 kg (FAOSTAT, 2011) with the highest consumption levels

in urban areas and lowest in pastoral rangeland areas (CIESIN, 2011) (Figure 3.6).

Figure 3.5 Average pig densities in Uganda show production specific production foci in Mbale, peri-urban Kampala, Kasese and

Masaka. Source: Robinson et al. (2014). Category thresholds are as accurate as 14 decimals.

Figure 3.6 Spatial distribution of per capita pig meat consumption, based on population density. Source: Center for International

Earth Science Information Network (CIESIN), 2011. Category thresholds are as accurate as 14 decimals.

24


3.3 Study site selection and characteristics

While in the long term, research findings are to be extrapolated and interventions scaled up and

out to the whole of Uganda, the CRP L&F selected three districts for initial smallholder pig value

chain scoping, assessment and piloting interventions. The process was completed in 2012 and

involved

3.3.1 Geographical targeting using GIS characterization by utilizing existing spatial data

(Van De Steeg et al., 2011). Candidate districts were established and classified into

value chain domains. The pre-selection of districts was based on data overlays of pig

population density and poverty levels. The time needed to reach the nearest urban

centre served as a proxy for market access and played an important role in classifying

the districts into different value chain domains. These are based on the time needed to

reach the nearest urban centre with a human population of at least 50,000 and describe

the spatial dimensions of production and consumption of pork: rural production for

rural consumption (rural-rural, RR), rural production for urban consumption (rural-

urban, RU) and urban production for urban consumption (urban-urban, UU).

3.3.2 Stakeholder consultation of step 3.3.1 and definition of soft selection criteria (based

on local knowledge) during a site selection workshop (Ochola, 2012). Stakeholders

critically discussed how poverty levels in some districts may be biased because there

are great gaps between rich and poor. For Masaka district, for instance, the overall

poverty levels seem to be low but it was emphasized that many farmers in the rural

areas are poor but the average poverty levels are raised by the number of wealthy people

in the urban areas. Other criteria such as the number of female-headed households,

levels of HIV/Aids, cross-border trade, market demand, seasonality of market access

and partnerships were thought necessary to be considered in site selection. From the

discussion, some criteria were added: potential partnerships, disease burden in pigs,

presence/access of input and service providers, and geographical access all year round.

At the end of the workshop the participants were asked to vote by scoring the relation

suitability of each candidate district established in 3.3.1 against the four soft criteria;

voting excluded ILRI and other CGIAR staff or affiliates.

Masaka, Mukono and Wakiso districts were voted the top three. Wakiso and Mukono districts are

both in close proximity to Kampala and are both considered peri-urban (UU value chain domain);

the participants therefore agreed to select Mukono, while Wakiso was omitted to include Kamuli

district which represents the typical RR value chain domain. The final districts selected are shown

in Figure 3.7. A Minimum validation checklist was administered in villages across the selected

districts between November and December 2012 (ILRI, 2012d). The objective was to validate if

preselected sites fit into the defined value chain domains as assumed in the steps above, and to

gather more information on sub-county and village data that could inform the finalization of the

value chain assessment tools. The final sites selected are listed in Table 3.1. Table 3.2 outlines

major characteristics of the selected districts.

25


Figure 3.7 The CRP L&F study sites selected in 2012: Masaka and Mukono districts in the Central region; Kamuli district in the

Eastern region of Uganda (ILRI/Pamela Ochungo).

Table 3.1 The final sites selected for the pig value chain assessment under the CRP L&F. Source: Poole et al. (2015).

District Sub-county Dominant value chain domain No. of villages selected

Masaka Kkingo RR 3

Kyanamukaka RR 3

Kabonera RU 3

Kimanya-Kyabakuza UU 2

Katwe-Butego UU 2

Nyendo-Ssenyange UU 2

Kamuli Kitayunwa RR 2

Namwendwa RR 2

Bugulumbya RR 4

Mukono Mukono town council UU 2

Goma UU 2

Kyampisi RU 4

Ntenjeru RR 4

26


Table 3.2 Characteristics of the sites selected by the CRP L&F. Sources: MAAIF/UBOS (2009); Twinomujini et al. (2011).

District Kamuli Masaka Mukono

Region Eastern Central Central

Area in sq km 1,154 2,1967 4,125

Human population

estimate (density

per sq km)

281,800

(181)

239,700

(109)

498,500

(120)

Estimated number

of pigs

55,989 236,150

(highest in Central region)

172,428

Livelihood

activities

Mainly agriculture-based:

Food crops: Soya bean, maize,

sorghum, cassava, sweet

potatoes, finger millet, rice,

groundnuts, simsim (sesame)

and sunflower.

Cash crops: Cotton, coffee and

sugar cane.

Vegetables: Tomatoes, onions

and cabbage.

Industry:

Manufacture of jiggery, brick

making, maize milling and

cotton ginning.


Food crops: Sweet potatoes,

bananas, beans, maize,

cassava, groundnuts, soya

bean, sorghum and finger

millet.

Cash crops: Coffee, cotton

and maize.

Fruits and vegetables:

Pineapples, tomatoes, onions

and cabbage.

Livestock farming.

Fishing on Lake Victoria.

Industry:

Manufacture of cassava

starch, curry powder,

garments, animal feeds, soft

drinks, footwear, laundry

soap, metal work, furniture,

jiggery, processing of tea,

coffee, hand weaving, glass

making and cotton ginning.


Food crops: Cassava, sweet

potatoes, beans, maize, finger

millet, groundnuts, soya bean,

bananas, sorghum, simsim

(sesame), cow peas, pigeon

peas and yams.

Cash crops: Cotton, coffee,

sugar cane and tea.

Fruits and vegetables:

Tomatoes, onions,

pineapples, vanilla, chillies,

passion fruit and cabbage.

Dairy farming.

Fishing on Lake Victoria.

Industry:

Processing of coffee, tea,

cocoa, sugar; manufacture of

textiles, animal feeds, beer,

boats, furniture, metal

products and grain milling.

7 While the map in Figure 3.7 represents the old district boundaries, numbers in Table 3.2 are based on the 2010 district reform whose implementation overlapped with the launch of the research.

27


Chapter 4: Parasites as a production constraint

4 Parasites as a production constraint in smallholder pig production systems

(Publications I & II)

This chapter characterizes the smallholder pig production systems in the selected study sites,

documents husbandry practices and describes major constraints to pig health as perceived by the

pig farmers (publication I). It also summarizes base line information on the prevalence of major

gastrointestinal helminths and protozoa and factors correlating with increased presence

(publication II).

The first publication shows that expensive feeds and pig disease were reported to be the major

constraints to more productivity at farm as perceived by the farmers; disease causing 45-90% of

losses across the sites. Major diseases described by the farmers were based on clinical signs visible

to the farmers and included ASF and infestation with parasites, both gastrointestinal helminths and

sarcoptic mange. Other diseases causing losses mainly due to skin alterations and weight loss were

ectoparasites such as flies, lice, ticks and tungiasis (in Kamuli only). Piglet diarrhoea was also

widely distributed. With regards to parasite control, the majority of the farmers (93%) stated to

deworm their animals at least once, usually when the piglet enters the farm and a few days before

it is sold. For treatment they either call a local veterinary professional or buy the drugs and

administer them themselves. The most common anthelminthics used were albendazole and

ivermectin. Spraying with acaricides is practiced by 37% of the farmers. Cross-cutting constraints

to pig health at the production sites were lack of knowledge on pig management, especially on

managing disease prevention and treatment; how to formulate suitable feed rations; limited access

to animal health services; poor quality drugs and lack of capital to invest in improved housing.

Participatory methods were used for the assessments and included qualitative and semi-

quantitative tools such as proportional piling, listing, ranking, scoring, seasonal calendars, as well

as pair-wise comparison and problem-opportunity matrices. Two facilitators fluent in the local

languages Luganda (spoken in Masaka and Mukono districts) and Lusoga (spoken in Kamuli

district) were trained on the tools, and after pre-testing them with a group of farmers, they

conducted the group sessions in all 35 selected villages. Pig health was only one component

researched during the value chain assessments; other aspects covered were pig feeding and

breeding, marketing as well as food safety and nutrition. These have been published separately.

The second publication reports findings from a cross-sectional survey in 21 of the 35 villages

where the participatory value chain assessments were held approximately five months prior to the

sampling. A random sample was taken between April and July 2013, and investigated the

prevalence of common nematode and trematode eggs, and coccidian oocysts in faecal samples

from 932 pigs by means of combined sedimentation-flotation method. The majority (61.4%) of all

pigs were found infected with at least one species of gastrointestinal helminths: 57.1% strongyles,

7.6% Metastrongylus spp., 5.9% Ascaris suum, 4.2% Strongyloides ransomi, and 3.4% Trichuris

suis. Coccidia oocysts were found in 40.7% of the sampled pigs, with significantly higher levels

in the more urban Mukono district. None of the animals showed infection with Balantidium coli

or Fasciola hepatica. A logistic regression model showed that routine management factors had a

greater impact on the prevalence of infection than regular treatment or the level of confinement.

Factors negatively correlating with gastrointestinal helminth infection were routine manure

removal, and the routine use of disinfectants.

28

Chapter 4: Parasites as a production constraint

Full details of the scientific findings of this chapter have been subjected to peer review and

published as original research papers in Preventive Veterinary Medicine and Parasitology

Research. In compliance with the copyright transfer statement to Elsevier and Springer-Verlag

Berlin Heidelberg, copies of the published articles appear overleaf. The final publications, together

with the supplementary material published electronically, are available online:

Dione, M. M., Ouma, E.A., Roesel, K., Kungu, J., Lule, P., Pezo, D. 2014. Participatory

assessment of animal health and husbandry practices in smallholder pig production systems in

three high poverty districts in Uganda. Prev Vet Med. 2014 Dec 1;117(3-4):565-576. doi:

10.1016/j.prevetmed.2014.10.012. Erratum in: Prev Vet Med. 2015 May 1;119(3-4):239.

Roesel, K., Dohoo, I., Baumann, M., Dione, M., Grace, D., Clausen, P.-H. 2017. Prevalence and

risk factors for gastrointestinal parasites in small-scale pig enterprises in Central and Eastern

Uganda. Parasitol Res. [2016 Oct 26; Epub ahead of print] 116: 335-345. doi: 10.1007/s00436-

016-5296-7

29

Chapter 4: Publication I

30-41

Michel M. Dione, Emily A. Ouma, Kristina Roesel, Joseph Kungu,Peter Lule, Danilo Pezo

Preventive Veterinary Medicine, Vol. 117, Dec. 2014, Issues 3-4, Pages 565-576 DOI: 10.1016/j.prevetmed.2014.10.012

http://dx.doi.org/10.1016/j.prevetmed.2014.10.012

You have to purchase this part online.

Participatory assessment of animal health and husbandrypractices in smallholder pig production systems in three highpoverty districts in Uganda

© 2014 Elsevier B.V. All rights reserved.


Chapter 4: Publication I, Corrigendum

42

Original article: http://dx.doi.org/10.1016/j.prevetmed.2014.10.012.

Michel M. Dione, Emily A. Ouma, Kristina Roesel, Joseph Kungu,Peter Lule, Danilo Pezo© 2015 Elsevier B.V. All rights reserved.

Preventive Veterinary Medicine, Vol. 119, May 2015, Issues 3-4, Page 239 DOI: 10.1016/j.prevetmed.2015.03.010


You have to read this part online.

Corrigendum

Corrigendum to “Participatory assessment of animal healthand husbandry practices in smallholder pig productionsystems in three high poverty districts in Uganda”

ht tp://dx.doi.org/10.1016/j.prevetm. ed.2014.10.012


Chapter 4: Publication II

43-53

Parasitology Research, January 2017, Vol. 116, Issue 1, pp 335-345 DOI: 10.1007/s00436-016-5296-7

http://dx.doi.org/10.1007/s00436-016-5296-7

You have to read this part online.

healthPrevalence and risk factors for gastrointestinal parasitesin small-scale pig enterprises in Central and Eastern Uganda

© The Author(s) 2016. This article is published with open access at Springerlink.com

Kristina Roesel, Ian Dohoo, Maximilian Baumann,Michel Dione, Delia Grace, Peter-Henning Clausen

http://dx.doi.org/10.1007/s00436-016-5296-7

http://dx.doi.org/10.1007/s00436-016-5296-7

Chapter 5: Parasites with implications for public health

5 Parasites with potential implications for public health (Publications III & IV)

This chapter presents the findings on the presence of two pig pathogens that are of global veterinary

public health importance: Trichinella spp. and Toxoplasma (T.) gondii. These two parasitic

infections have never been studied in pigs in Uganda, and we hope that our findings will inform

the pig industry and the planning of future in-depth investigations. The prevalence data refers to

the same cohort of pigs for which gastrointestinal parasite infection rates were presented in chapter

4.

The overall prevalence of Trichinella-specific antibodies was 6.9% out of 1,125 sampled animals

but showed significantly higher levels in value chain types with a rural origin of production (p <

0.05). Kamuli district, where the RR value chain type dominates showed a significantly higher

ELISA-prevalence than the more urban Masaka and Mukono districts (p < 0.001). For the first

time, a study in pigs in sub-Saharan Africa was able to confirm 31 % ELISA-positive samples by

Western Blot. Isolation of infective first-stage larvae from 499 samples in ELISA clusters to

identify the dominating Trichinella spp. was not successful. Due to the large sample size, we are

confident that even if domestic pigs are infected, the larval burden would be too low to pose a

major risk to consumers for developing trichinellosis.

T. gondii-specific antibodies were found in 28.7% of the animals using a commercial ELISA kit;

village herd prevalence was 100%. Significantly higher levels were shown for Masaka and

Mukono districts compared to rural Kamuli districts; and univariate analysis showed that pigs

raised in urban production settings (UU value chain types) showed significantly higher levels of

seropositivity than animals of a rural production origin (RR and RU value chain types) (p < 0.007).

Full details of the scientific findings of this chapter have been subjected to peer review, the work

on Trichinella was published as original paper in PLOS ONE (publication III). In compliance with

the copyright transfer statement to the Public Library of Science (PLOS), a copy of the article

appears overleaf. The final publication, together with the supplementary material published

electronically, is available online:

Roesel, K., Nöckler, K., Baumann, M.P.O., Fries, R., Dione, M.M., Clausen, P.-H., Grace, D. First

Report of the Occurrence of Trichinella-Specific Antibodies in Domestic Pigs in Cetral and

Eastern Uganda. 2016 Nov 21;11(11):e0166258. doi: 10.1371/journal.pone.0166258

The work on the occurrence of porcine T. gondii infections and related risk factors (publication

IV) has been accepted for presentation to a peer audience by the scientific committee of the First

Joint Conference of the Association of Institutions for Tropical Veterinary Medicine (AITVM)

and the Society of Tropical Veterinary Medicine (STVM). An author-created version of the

abstract appears overleaf and is available online:

Roesel, K., Schares, G., Grace, D., Baumann, M., Fries, R., Dione, M., Clausen, P.-H. 2016. The

occurrence of porcine Toxoplasma gondii infections in smallholder production systems in Central

and Eastern Uganda. In: Clausen, P.-H., Baumann, M., Nijhof, A. (eds), Tropical Animal Diseases

and Veterinary Public Health: Joining Forces to Meet Future Global Challenges. First Joint

ATIVM-STVM Conference, Berlin, Germany, 4-8 September 2016. Giessen, Germany: Verlag der

DVG Service GmbH. Page 22.

54

Chapter 5: Publication III

55

RESEARCH ARTICLE

First Report of the Occurrence of Trichinella-

Specific Antibodies in Domestic Pigs in Central

and Eastern Uganda

Kristina Roesel1,2*, Karsten Nockler3, Maximilian P. O. Baumann4, Reinhard Fries5¤,

Michel M. Dione6, Peter-Henning Clausen1, Delia Grace2

1 Institute for Parasitology and Tropical Veterinary Medicine, Department of Veterinary Medicine, Freie

Universitat Berlin, Berlin, Germany, 2 Food safety and zoonoses program, International Livestock Research

Institute, Nairobi, Kenya, 3 Department Biological Safety, Federal Institute for Risk Assessment, Berlin,

Germany, 4 FAO Reference Centre for Veterinary Public Health, Department of Veterinary Medicine, Freie

Universitat Berlin, Berlin, Germany, 5 Institute for Meat Hygiene, Department of Veterinary Medicine, Freie

Universitat Berlin, Berlin, Germany, 6 Animal science for sustainable productivity program, International

Livestock Research Institute, Kampala, Uganda

¤ Current address: Private residence, Obernkirchen OT Krainhagen, Germany

* [email protected]

Abstract

Previous research on trichinellosis in Africa focused on isolating Trichinella from wildlife

while the role of domestic pigs has remained highly under-researched. Pig keeping in

Uganda is historically recent, and evidence on zoonotic pig diseases, including infection

with Trichinella species, is scarce. A cross-sectional survey on Trichinella seroprevalence in

pigs was conducted in three districts in Central and Eastern Uganda from April 2013 to Janu-

ary 2015. Serum from a random sample of 1125 pigs from 22 villages in Eastern and Central

Uganda was examined to detect immunoglobulin G (IgG) against any Trichinella spp. using

a commercially available ELISA based on excretory-secretory antigen. ELISA positive sam-

ples were confirmed using Western Blot based on somatic antigen of Trichinella spiralis as

recommended in previous validation studies. Diaphragm pillar muscle samples (at least 5 g

each) of 499 pigs from areas with high ELISA positivity were examined using the artificial

digestion method. Overall, 78 of all 1125 animals (6.9%, 95% CI: 5.6–8.6%) tested positive

for antibodies against Trichinella spp. in the ELISA at significantly higher levels in Kamuli

district compared to Masaka and Mukono districts. Thirty-one percent of the ELISA positive

samples were confirmed IgG positive by the Western Blot leading to an overall seropreva-

lence of 2.1% (95% CI: 1.4–3.2%). The large proportion of ELISA positive samples that

could not be confirmed using Western blot may be the result of cross-reactivity with other

gastrointestinal helminth infections or unknown host-specific immune response mecha-

nisms in local pig breeds in Uganda. Attempts to isolate muscle larvae for species determi-

nation using the artificial digestion method were unsuccessful. Due to the large number of

muscle samples examined we are confident that even if pigs are infected, the larval burden

in pork is too low to pose a major risk to consumers of developing trichinellosis. This was the

first large systematic field investigation of Trichinella infection in domestic pigs in Uganda

PLOS ONE | DOI:10.1371/journal.pone.0166258 November 21, 2016 1 / 16

a11111

OPENACCESS

Citation: Roesel K, Nockler K, Baumann MPO,

Fries R, Dione MM, Clausen P-H, et al. (2016) First

Report of the Occurrence of Trichinella-Specific

Antibodies in Domestic Pigs in Central and Eastern

Uganda. PLoS ONE 11(11): e0166258.

doi:10.1371/journal.pone.0166258

Editor: Alejandro Escobar-Gutierrez, Instituto de

Diagnostico y Referencia Epidemiologicos,

MEXICO

Received: July 18, 2016

Accepted: October 25, 2016

Published: November 21, 2016

Copyright: © 2016 Roesel et al. This is an open

access article distributed under the terms of the

Creative Commons Attribution License, which

permits unrestricted use, distribution, and

reproduction in any medium, provided the original

author and source are credited.

Data Availability Statement: Data are available

from Figshare: DOI:10.6084/m9.figshare.4219635;

URL https://figshare.com/articles/Trichinella_

Uganda_data_for_PLOS_ONE_final_xls/4219635.

Funding: The field research was funded by the

CGIAR Research Program on Agriculture for

Nutrition and Health, led by the International Food

Policy Research Institute (http://www.ifpri.org/

division/agriculture-nutrition-and-health-a4nh), the

Safe Food, Fair Food project funded by the Federal

Ministry for Economic Cooperation and


56

and its results imply that further studies are needed to identify the Trichinella species

involved, and to identify potential sources of infection for humans.

Introduction

Human trichinellosis is acquired through the ingestion of the first-stage larvae of the nematode

Trichinella in raw or undercooked meat from domestic animals, mainly pigs, and game. Clini-

cally relevant infections can initially cause diarrhoea and abdominal pain; subsequently,

migrating larvae and their metabolites may provoke fever, facial oedema and myalgia, or even

fatal myocarditis. The severity of the symptoms may depend on the infection dose and the Tri-chinella spp. causing the infection [1].

The nematode Trichinella is cosmopolitan and found everywhere except the Antarctica.

Eight species and four genotypes have so far been documented, five of them in Africa: T. brit-ovi in North and West Africa, Trichinella T8 in Namibia and South Africa, T. nelsoni in Eastern

and South Africa, T. zimbabwensis in Southern and Eastern Africa and T. spiralis in Egypt [2–

5]. While a wide range of host species can be infected (mammals, birds and reptiles), only

humans show clinical signs in case of infection [1]. While human infection is strictly related to

the consumption of raw or undercooked infected meat [3], the major risk factors associated

with infection in pigs are the ingestion of infectious first-stage larvae by scavenging, or feeding

on scraps from pig slaughter or game hunting [6].

Most previous research on trichinellosis in Africa focused on isolating Trichinella from

wildlife [7–13], and it was long believed that in Africa, Trichinella infection essentially affects

wild carnivores [14] and that pigs are not infected with Trichinella in East Africa. Outbreaks of

human trichinellosis in Africa date back several decades and were documented in Egypt [15],

Northwest Ethiopia [16,17], Kenya [18] and Tanzania [19]. Other cases have been diagnosed

in France in travellers returning from Senegal [20], a patient in Japan after travelling to Kenya

[21], and travellers returning to the United States of America from Africa [22]. These cases of

human trichinellosis have been mostly associated with the consumption of game meat, espe-

cially bush pig (Potamochoerus sp.) and warthog (Phacochoerus sp.). The prevalence in wildlife

by regions and countries in Africa has been synthesized in recent reviews [5,8] but the real

prevalence of human trichinellosis in Africa in general, and Uganda in particular, remains

unknown.

Only two studies on Trichinella-specific antibodies in domestic pigs in sub-Saharan Africa

have been published, both from Nigeria, and reporting seroprevalences of 40% (48/120) [23]

and 11% (49/450) [24]. Attempts to directly detect muscle larvae from potentially naturally

infected domestic pigs have been made in Northern Tanzania [25] and Ghana [26], but unsuc-

cessfully. However, in Egypt, where T. spiralis had previously been documented, muscle larvae

could be isolated by means of artificial digestion [15,27].

In sub-Saharan Africa, human population is growing rapidly and urbanization is increasing

while most of the food is produced in the rural areas by smallholder farmers. Pig keeping has

become a popular income-generating activity across Eastern Africa. However, pigs are not a

traditional livestock species in the region and, in Uganda, evidence on zoonotic pig diseases

has been scarce and limited to pigs as a reservoir for Trypanosoma species as well as the natural

intermediate host for Taenia solium [28]. The presence of porcine Trichinella infection in

Uganda was reported to the World Organisation for Animal Health (OIE) in 2008 but without

any further provision of details [29].

Trichinella and Domestic Pigs in Uganda


Development, Germany (grant no.: 81141843) in

cooperation with the CGIAR Research Program on

Livestock and Fish (https://livestockfish.cgiar.org/)

through the Smallholder Pig Value Chains

Development project in Uganda (funded by the

International Fund for Agricultural Development –

European Commission, grant no. COFIN-ECG-63-

ILRI). We also acknowledge the CGIAR Fund

Donors (http://www.cgiar.org/who-we-are/cgiar-

fund/fund-donors-2). The funders had no role in

study design, data collection and analysis, decision

to publish, or preparation of the manuscript.

Competing Interests: The authors have declared

that no competing interests exist.

57

The objectives of the present survey were to investigate if domestic pigs in Uganda are

exposed to Trichinella by means of indirect methods in order to estimate if consumers are at

risk of contracting trichinellosis through pork consumption.

Materials and Methods

Ethics statement

The research involved obtaining information from pig farmers and sampling of live animals as

well as meat sampling from butcheries. Approval was obtained from the Research and Ethics

Committee at the College of Veterinary Medicine, Animal Resources and Biosecurity, Maker-

ere University, Kampala (Ref.: VAB/REC/13/103) and from the Uganda National Council for

Science and Technology (Ref.: A 525). Informed consent was obtained from all individual par-

ticipants included in the study.

Study area

A cross-sectional survey was conducted in three districts in Central and Eastern Uganda from

April 2013 to January 2015. Uganda is located between 4˚N and 1˚S of the equator in East

Africa at the northern shores of Lake Victoria. Due to its proximity to the equator, the climate

is tropical savannah in most parts of the country with abundant vegetation and rainfall.

Despite its small size, the country’s fauna is extremely diverse [30] and located in more than 60

protected areas, including ten national parks, and more than 500 forest reserves.

Site selection

As part of a research for development project led by the International Livestock Research Insti-

tute (ILRI) and partners, Kamuli, Mukono and Masaka districts were selected with a range of

stakeholders. Details of the process and criteria are described elsewhere [31,32]. Based on the

2008 livestock census [33], four to six sub-counties with a high pig population were purpo-

sively selected, and villages were further categorized into value chain domains by means of a

checklist and consultation with local partners. Value chain domains describe the spatial

dimensions of production and consumption of pigs: rural production for rural consumption

(rural-rural, RR), rural production for urban consumption (rural-urban, RU) and urban pro-

duction for urban consumption (urban-urban, UU) [31]. In each district, two sub-counties

were purposively selected, and within each sub-county, two to three villages were randomly

selected. From a total of 35 villages [31], 22 villages were purposively selected for the present

prevalence study (Fig 1), based on available financial and logistic resources.

Sample size calculation

The original sample size was calculated to estimate district-level prevalence and considering

an infinite population using n = [Z2P(1–P)]/d2; where n is the required sample size; Z is the

multiplier from a standard normal distribution (1.96) at a probability level of 0.05; P is the esti-

mated prevalence which is most conservatively estimated to be 50% considering there is no ref-

erence data from pigs in the area under study; (1–P) is the probability of having no disease and

d is the desired precision level (5%). Therefore, a sample size of 384 pigs per district was

required for the study. To increase precision, a sample size of 400 pigs in each district was

planned.




58

Selection of the individual animals

In each of the 22 selected villages, a list of all households keeping pigs was generated in collabo-

ration with the local government. From that list, households were randomly selected and

invited to participate. Per household, one animal was selected for blood collection if it was

aged three months or older, not weak or emaciated, not pregnant, and did not have a litter less

than two months old.

Pigs were restrained using a snare and bled from the cranial vena cava using BD Vacutai-

ner1 needles and BD Vacutainer1 plain tubes. The blood samples were kept standing in an

ice box at 4˚C to avoid haemolysis. At the field laboratory, blood was centrifuged and serum

harvested into barcoded vials that were stored at -20˚C until processed at Makerere University

in Kampala, Uganda. Prior to shipment to Friedrich-Loeffler-Institute, Greifswald, Germany,

the samples were heat-inactivated at 56˚C for 20 minutes.

Fig 1. Twenty-two villages were selected for a multi-pathogen survey in pigs in three districts of Central and Eastern Uganda, April to July 2013.

(Pamela Ochungo/ ILRI)

doi:10.1371/journal.pone.0166258.g001




59

Enzyme-linked immunosorbent assay (ELISA)

A commercially available ELISA based on excretory-secretory (E/S) antigen was used to detect

immunoglobulin G (IgG) against any Trichinella spp. in pig sera (PrioCHECK1 Trichinella

Ab, Prionics AG, Wagisstrasse 27A, CH-8952 Schlieren). According to the manufacturer, the

PrioCHECK1 Trichinella Ab ELISA showed a sensitivity and specificity of 100% in an in-

house validation study [34].

The assay was performed according to the manufacturer’s instructions in a four-step proto-

col: serum was diluted 1:50 and incubated on plates coated with E/S antigen of Trichinella spir-alis; a peroxidase-labelled anti-pig IgG was used as a secondary antibody bound to the antigen;

a chromogen (TMB) substrate was added and the optical density of the sample was measured

by reading the test plate at 450 nm wavelength (Sunrise™ Tecan, powered by Magellan™ soft-

ware). The results were calculated in percent positivity (PP) in reference to the positive control

sample. Results at or above the manufacturer’s cut-off of 15% PP were considered ELISA

positive.

Confirmatory testing

It is recommended that ELISA positive samples are tested by Western Blot for confirmation of

the presence of IgG antibodies against Trichinella spp. [35,36]. While the ELISA was based on

E/S antigen, the Western Blot used for confirmatory testing in this study was based on somatic

antigen from crude worm extract (CWE) of Trichinella spiralis first-stage larvae [37]. In addi-

tion to all relevant protein fractions of the E/S antigen (43–45 and 66–67 kDa), it includes frac-

tions 47, 61, and 102 kDa which are Trichinella-specific [36]. In validation studies evaluating

CWE- against E/S-Western Blot and using artificial digestion as ‘gold standard’, the CWE--

Western Blot showed a sensitivity ranging from 95.8–91.1% and a specificity ranging from

99.5–100% [35,36]. In this study, it was performed on all ELISA positive samples, and a ran-

domly selected subset of ELISA negative samples (n = 16) for internal quality control. Sera that

showed an antibody reaction to any of the five immunogenic protein bands mentioned above

were considered Western Blot positive.

Artificial digestion

In an attempt to isolate Trichinella muscle larvae for species determination, 499 pig diaphragm

samples from four clusters with a high antibody prevalence based on the ELISA test were col-

lected from October 2014 to January 2015. Diaphragm muscle is the major predilection site

for Trichinella spp. in domestic swine [38,39]. Artificial digestion according to OIE instruc-

tions [40] was carried out at the Central Diagnostic Laboratory at the College of Veterinary

Medicine, Animal Resources and Biosecurity, Makerere University in Kampala, Uganda. A

positive control of Trichinella spiralis was provided by the National Reference Laboratory for

Trichinella hosted by the Federal Institute for Risk Assessment in Berlin, Germany.

Muscle samples of at least 5 g per animal were tested to increase sensitivity of the artificial

digestion method [37,39,41]; 102 samples weighed 5 g; 396 samples 10 g and one sample 20 g.

Up to 20 samples with a total weight of 100 g were examined in a pool by artificial digestion

method [40].

Household survey data

Using a structured questionnaire, information on self-reported husbandry and consumption

practices was collected at each household from where a pig was sampled.




60

Data management

ELISA results were exported to Microsoft Excel, Version 2010, from the ELISA reader using

Magellan™ software. Laboratory data from Western Blot and artificial digestion were entered

into Microsoft Excel, Version 2010. Household data were entered using Census and Survey

Processing System, Version 4.1. (U.S. Census Bureau), and subsequently exported to MySQL

for data validation. Datasets were merged for cleaning and descriptive analysis in STATA 13.1

(StataCorp).

Results

Antibody prevalence

Overall, 78 of 1125 animals (6.9%, 95% CI: 5.6–8.6%) tested positive for antibodies against Tri-chinella spp. in the ELISA (Table 1), with significant differences across districts (p< 0.001),

sub-counties (p< 0.05) and value chain types (p = 0.05) (Fig 2). Most ELISA positive samples

were found in Kamuli district, which is dominated by an RR value chain type, compared to

Mukono and Masaka districts.

Table 1. Prevalence estimates for anti-Trichinella IgG (PrioCHECK® Trichinella Ab) in three districts in Central and Eastern Uganda, sampled

between April and July 2013.

District Village Value chain typea Sample size (n) ELISA+ Prevalence estimateb (confidence limits)

Kamuli (1) Baluboinewa RR 46 3 6.5% (2.1–18.6%)

(2) Bukyonza B RR 28 4 14.3% (5.4–32.9%)

(3) Kantu zone RR 110 20 18.2% (12.0–26.6%)

(4) Ntansi RR 105 6 5.7% (2.6–12.2%)

(5) Butabala RR 39 1 2.6% (0.4–16.5%)

(6) Isingo A RR 65 16 24.6% (15.6–36.6%)

Total 393 50 12.7% (9.8–16.4%)

Masaka (7) Kyamuyimbwa-Kikalala RU 31 0 0%

(8) Butego RU 28 0 0%

(9) Kijjabwemi UU 41 0 0%

(10) Kyabakuza B UU 36 0 0%

(11) Kisoso RU 56 2 3.6% (0.9–13.4%)

(12) Ssenya RR 37 1 2.7% (0.4–17.3%)

(13) Kanoni-Bukunda RU 51 1 2.0% (0.3–12.9%)

(14) Lukindu RR 40 5 12.5% (5.2–27.0%)

(15) Ssenyange A UU 47 2 4.3% (1.1–15.7%)

Total 367 11 3.0% (1.7–5.3%)

Mukono (16) Dundu RU 56 2 3.6% (0.9–13.4%)

(17) Kyoga RU 52 1 1.9% (2.7–12.7%)

(18) Joggo RR 62 5 8.1% (3.4–18.1%)

(19) Kitete RR 54 2 3.7% (0.9–13.8%)

(20) Bugoye-Kabira RR 47 3 6.4% (2.1–18.2%)

(21) Kazo-Kalagala RR 51 0 0%

(22) Nsanja-Gonve RR 43 4 9.3% (3.5–22.5%)

Total 365 17 4.7% (2.9–7.4%)

Grand Total 1125 78 6.9% (5.6–8.6%)

aSpatial dimensions of production and consumption of pigs [31]: rural production for rural consumption (RR); rural production for urban consumption (RU);

urban production for urban consumption (UU)bCalculated at p = 0.05 and CI = 0.95

doi:10.1371/journal.pone.0166258.t001




61

Twenty-four (30.8%) of the 78 ELISA positive samples were confirmed IgG positive by the

Western Blot leading to an overall seroprevalence of 2.1% (95% CI: 1.4–3.2%) (Fig 3 and

Table 2). There were no significant differences in the Western Blot prevalence between dis-

tricts (Fig 4). However, the proportion of confirmed samples showed a reverse order with

most ELISA positive samples confirmed in Mukono district (47%), followed by Masaka (36%)

and Kamuli (24%) districts. All ELISA negative samples used for internal quality control tested

negative in the Western Blot.

Artificial digestion

A total of 499 diaphragm samples were collected from 32 butcheries, representing all butcher-

ies operating in the four sub-counties with the highest ELISA prevalence at the time of sam-

pling. Trichinella muscle larvae were not detected in any of the samples.

Descriptive analysis

Two-thirds of the households participating in the survey were male-headed (67.0%) with a

more equal ratio (60:40) in Masaka district. The majority of the households in the study were

Fig 2. Prevalence estimates and confidence levels for anti-Trichinella IgG (PrioCHECK Trichinella Ab) in three districts in Central and

Eastern Uganda, sampled between April and July 2013.





62




63

members of the Christian faith (94.0%) and four pig keeping households (0.4%) in Masaka

and Mukono districts were headed by Muslims. In all districts, the most commonly found

herd size was two to five pigs (39.4% of households); households keeping only one pig were

more common in rural Kamuli (28.5%), while in Masaka and Mukono districts, keeping six to

ten pigs was more frequent. The most commonly reared breeds (58.3%) were crosses between

the so-called local (black) and exotic (i.e. Large White, Camborough) breeds.

Most of the animals (76.7%) were raised in rural settings. According to the ILRI value chain

classification, 30.5% of the pigs kept in rural areas were destined for sale at urban markets

(RU) while the rest were intended to be marketed locally (RR). More than half of the house-

holds kept their pigs tethered or confined (53.5% and 52.7%, respectively), and only a small

fraction left their pigs roam free (2.1%). Tethering was the preferred method of restricting the

movement of pigs in Kamuli and Mukono districts, while in Masaka almost three-quarters of

pig farmers kept their pigs confined. Overall, all pig farming households fed mixed pig rations,

utilizing crop residues (98.3%) and commercial feeds (70.9%), while 35.0% practised swill feed-

ing (e.g. kitchen or restaurant leftovers and wasted bread). More than half of the pig farming

households (52.9%) performed routine pest/rodent control.

Direct and indirect contact with wild animals was proxied by reports of wildlife sightings in

the village (34.9% of pig farmers). However, only 4.1% of pig farmers reported that they con-

sumed game meat. Those who did ate meat from antelopes such as Sitatunga (Tragelaphus spe-kii) or Ugandan Kob (Kobus kob thomasi), but also rodents such as cane rats (Thryonomysspp., locally referred to as “edible rats”), or Canidae including stray dogs (Canis familiaris) and

civet cats (Viverridae) as well as wild pigs (Potamochoerus spp.), buffaloes (Syncerus caffer),hares (Leporidae) and guinea fowls (Numididae).

Slaughtering pigs at home was more frequent in Masaka and Mukono districts. Overall,

only 12.6% of pig farmers slaughtered at home at least once a year; the majority (71.2%) never

slaughtered their own pigs (Table 3). Of those farmers who slaughtered at home, more than

three-quarters reported that the meat had never been inspected. At slaughter, viscera and

intestinal contents were usually buried, thrown into the bush or given to dogs. Most of the pig

farmers in the study area were also pork consumers and ate pig meat at least once a month

(57.8%), while 21.7% never consumed pork and 15.4% ate it only occasionally. The most fre-

quent mode of processing the meat was frying (62.9%) or boiling (37.7%) (Table 3).

Discussion

The present survey is one of the few in sub-Saharan Africa and the first in Uganda to investi-

gate the occurrence of infection with Trichinella spp. in domestic pigs. To the authors’

Fig 3. Four of the 78 ELISA positive samples tested by Western Blot based on somatic antigen (strip

18–21). Strip 22 represents the positive control and strip 23 the negative control.


Table 2. Western Blot (WB) confirmation of ELISA positive samples (anti-Trichinella IgG), collected between April and July 2013 in 22 villages

from three districts in Central and Eastern Uganda.

District Sample size (n) ELISA+ WB- WB+ Total confirmed (%) WB prevalence estimatea (confidence limits)

Kamuli 393 50 38 12 24.0 3.1% (1.7–5.3%)

Masaka 367 11 7 4 36.4 1.1% (0.4–2.9%)

Mukono 365 17 9 8 47.1 2.2% (1.1–4.3%)

Total 1125 78 54 24 30.8 2.1% (1.4–3.2%)

WB: Western BlotaCalculated at p = 0.05 and CI = 0.95





64

knowledge, it is also the first investigation in Africa confirming ELISA positive results by

Western Blot that resulted in an overall seroprevalence of 2.1%.

Two farm surveys in Nigeria found a prevalence of Trichinella IgG of 10.9% [24] and 40%

[23]. Both surveys used the same commercial ELISA based on E/S antigens as in the present

survey but reported higher prevalence rates. In previous studies, this ELISA detected antibod-

ies in samples with larval densities of 0.025 larvae per gram (LPG) [42]. The authors of those

validation studies were also able to detect antibodies in pigs infected with different Trichinellaspecies, like T. spiralis, T. britovi and T. pseudospiralis, but showed no cross-reactivity with

other pig pathogens such as Trichuris suis, Oesophagostomum, Strongyloides, Hyostrongylus,Oesophagostomum/Hyostrongy lus and Salmonella typhimurium [34]. T. nelsoni, a Trichinellaspecies previously reported in game animals in Eastern Africa, has not been included in those

validation studies.

ELISAs of the preceding generation were based on somatic antigen of Trichinella spiralis.Since then, the specificity of the ELISA has been improved by utilizing E/S antigens obtained

from metabolites of Trichinella muscle larvae incubated in vitro [37]. While the manufacturer

of the commercial kit used in this study reports a sensitivity and specificity of 100% [34], a

comparable in-house ELISA for the detection of Trichinella-specific antibodies had a test

Fig 4. Proportion of ELISA positive samples confirmed by Western Blot based on somatic antigen of Trichinella spiralis in three districts

in Central and Eastern Uganda, sampled between April and July 2013.





65

sensitivity and specificity of 96.8% and 97.9%, respectively [36]. As shown in other studies,

unspecific cross-reactions may not be fully excluded; therefore, a Western Blot was used for

confirmatory testing. Reportedly, the combined use of both serological methods shows a sensi-

tivity that is 31.4 times higher than that of the digestion assay [43], especially in naturally

infected wild pigs with a lower larval burden. Western Blot based on somatic antigen allows

Table 3. Pig slaughter, processing and consumption practices in Central and Eastern Uganda (2013).

Variable Totals n (%)

Frequency of home slaughter

�Once a month 26 (2.74%)

�Once a year 71 (7.49%)

�Once a year 22 (2.32%)

Never 675 (71.20%)

Cannot remember/don’t know 9 (0.95%)

Missing 145 (15.30%)

Total 948 (100.00%)

Frequency of meat inspection at home slaughter (if practiced)

Always 7 (5.88%)

Sometimes 9 (7.56%)

Cannot remember/don’t know 2 (1.68%)

Never 93 (76.15%)

Missing 8 (6.72%)

Total 119 (100.00%)

Disposal of viscera & intestinal contents

Throw away outside compound 17 (1.79%)

Throw away inside compound 2 (0.21%)

Manure 0

Feed the live pigs 0

Other: buried 28 (2.95%)

Other: given to dogs 12 (1.27%)

Other: given to people 2 (0.21%)

Other: not specified 81 (8.54%)

Missing 806 (85.02%)

Total 948 (100.00%)

Frequency of pork consumption

�Once a month 548 (57.81%)

�Once a year 146 (15.40%)

�Once a year 32 (3.38%)

Never 206 (21.73%)

Missing 16 (1.69%)

Total 948 (100.00%)

Pork preparation

Boiling 357/948 (37.66%)

Frying 596/948 (62.87%)

Barbeque 95/948 (10.02%)

Other 7/948 (0.74%)

Missing 213/948 (22.47%)

Consumption of game meat

39/948 (4.11%)





66

discriminating ELISA positive samples further because it includes all relevant protein fractions

of the E/S antigen (43–45 and 66–67 kDa) and fractions 47, 61 and 102 kDa which are Trichi-nella-specific [35,36]. The obvious discrepancy between ELISA positives and Western Blot

positives may be the result of cross-reactivity with other gastrointestinal helminth infections as

found in this study for co-infection with strongyle species (data not shown). It could also be

caused by unknown host-specific immune response mechanisms in local pig breeds from

Uganda because the validation studies involved European pig breeds.

We were not able to determine the Trichinella species infecting domestic pigs in the investi-

gated study areas of Uganda as artificial digestion of a large number of muscle samples did not

result in the isolation of muscle larvae. Infectivity and larval burden in domestic pigs largely

depends on the Trichinella species. While T. spiralis has a very high reproductive capacity

resulting in 427.4 LPG five weeks p.i., T. nelsoni and T. britovi result in a larval burden of 52.2

and 38.0 LPG, respectively [44]. This may explain why potentially low larval burdens of a non-

T. spiralis infestation in the muscle could not be detected by artificial digestion. For future

studies, testing larger amounts (up to 50–100g) of muscle tissue may compensate for a possible

decrease in sensitivity [40] due to unknown larval burden in predilection sites. In addition,

future sampling studies to detect larvae should concentrate in areas where seroprevalence was

highest by Western Blot. This was not applicable in this study due to logistics and timing of

sampling and testing.

While the Nigerian survey by Momoh et al. [23] reported potential risk factors, we deliber-

ately waived statistical risk factor analysis in our study. We performed Western Blot as a con-

firmatory test which reduced the number of positive samples by 69% and left us with too few

positives to conduct sound univariate analysis. Confirmation by Western Blot has not been

done in previous studies in domestic pigs in Africa where ELISA positivity was used as the out-

come variable and the number of observations was much higher. In the present study, the out-

come variable would ideally be the result of the Western Blot. In this study, 78 samples tested

ELISA positive and 24 were confirmed as Western Blot positive; 1047 samples tested ELISA

negative but an unknown number could be Western Blot positive. Since we had only sufficient

funding to carry out Western Blot on a subset of 16 ELISA negative samples, and although all

were negative in Western Blot, it is not possible to definitively identify which (if any) of the

untested 1031 ELISA negative samples would have tested positive or negative in Western Blot.

Thus, conducting a risk factor analysis on the small subset of ELISA positive samples was not

considered meaningful as the relation between ELISA positive, Western Blot positive, ELISA

negative and Western Blot negative samples was not known, and risk factor analysis would

then only apply to a small subset of pigs of unknown epidemiological status.

From the information gathered in this survey, potential reservoirs for Trichinella sp. such as

rodents and stray dogs should be investigated in the future. They may act as potential links

between the sylvatic and domestic life cycle as shown by researchers in Egypt who isolated

muscle larvae from dogs and rodents in urban settings and in the proximity of abattoirs

[45,46].

Information gathered on slaughter and consumption practices are indicative but not con-

clusive. However, previous reports in the same geographical area suggest that pig farmers do

not consume raw pork but thoroughly heat meat products [47]. Results on slaughter practices,

for instance, disposal of remains, or the consumption of game meat, are likely to be underre-

ported by the participants of the present survey. The frequency of wildlife sightings, too, may

be underreported as wildlife is very common in some areas and often only subconsciously

noticed as it is such an integral part of daily life.

Previous reviews suggest that Trichinella infection in pigs and people plays a negligible role

in Africa because the people of sub-Saharan Africa consist mainly of Bantu origin who do not




67

consume meat [6,48]. Personal observation of an increasing number of roasted meat outlets

(both pork and beef) and Food and Agriculture Organization of the United Nations statistics

on per capita consumption of meat [49] strongly disagree with this argument. In Uganda, pig

numbers increased more than tenfold from 200,000 to more than 3 million since the 1980s

[33], while per capita consumption is highest in Eastern Africa at 3.4 kg [49] at increasing

trends. In general, the history of the domestic pig in Africa is highly controversial and has

been heavily neglected in research [50]. Uganda in particular is a very diverse country with

Muslims and Christians intermarrying and a substantial inflow of migrants, especially from

China and India [51], who traditionally consume a lot of pork and may contribute to an

increased demand in the near future.

In conclusion, we were able to demonstrate that domestic pigs in Kamuli, Masaka and

Mukono districts in Uganda have been infected with Trichinella spp. This was the first large

systematic investigation of Trichinella infection in domestic pigs in Uganda, potentially identi-

fying high-risk areas through the confirmation of ELISA positive samples using Western Blot.

We were not able to identify the species; however, this was not the objective of the study. Due

to the large number of diaphragm muscle samples examined at higher sample weight (at least

5 g), we are confident that even if pigs are infected, the larval burden in pork is too low to pose

a major risk to consumers of developing trichinellosis. Further studies are needed to identify

the Trichinella species infecting domestic pigs and to identify potential sources of infection

and modes of transmission.

Acknowledgments

We thank Dr. Joseph Erume, Dr. Joseph Kungu, Ms. Joyce Akol, Ms. Angella Musewa and Mr.

Dickson Ndoboli for the support provided during the farm survey and sample processing as

well as Mr. Edward Mawanda, Mrs. Milly Nanyolo and Mr. Joseph Sserwadda for facilitating

the collection of pork samples from butcheries. In addition, the authors are grateful for the

technical support provided by Dr. Gereon Schares and his staff at Friedrich-Loeffler-Institute

for the provision of the laboratory facilities and capacity building as well as Mr. Peter Bahn at

the Federal Institute for Risk Assessment for facilitating the confirmatory testing, Dr. Ian

Dohoo for his advice on data analysis, and Ms. Tezira Lore, ILRI communication specialist, for

proof-reading the manuscript. We extent our gratitude to the field veterinary staff and all pig

farmers in Masaka, Mukono and Kamuli districts for their active participation throughout the

field survey.

Author Contributions

Conceptualization: KR KN MB RF PHC.

Data curation: KR MD.

Formal analysis: KR.

Funding acquisition: DG.

Investigation: KR MD.

Methodology: KR KN MB RF MD PHC DG.

Project administration: KR DG.

Resources: KN MB RF PHC DG.

Software: DG.




68

Supervision: KN MB RF PHC.

Validation: KR KN MB RF PHC MD DG.

Visualization: KR KN.

Writing – original draft: KR.

Writing – review & editing: KN MB RF MD PHC DG.

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Chapter 5: Publication IV

The occurrence of porcine Toxoplasma gondii infections in smallholder production systems

in Central and Eastern Uganda

Kristina Roesel1,2, Gereon Schares3, Delia Grace2, Maximilian Baumann4, Reinhard Fries4, Michel

Dione2, Peter-Henning Clausen1

1Institute for Parasitology and Tropical Veterinary Medicine, Freie Universität Berlin, Germany

2International Livestock Research Institute (ILRI), Kampala, Uganda and Nairobi, Kenya

3Friedrich-Loeffler-Institute, Greifswald, Germany

4FAO Reference Centre for Veterinary Public Health, Freie Universität Berlin, Germany

Abstract

Pig production is an emerging agribusiness in Eastern Africa but baseline information on pig

diseases including zoonoses is still scarce. Infection with Toxoplasma gondii does not usually

present with clinical signs in pigs, yet it is considered an important source of human infection

when pork containing tissue cysts is poorly handled or consumed raw or undercooked.

In a cross-sectional survey between April and July 2013, we sampled 932 pigs between three

months to three years of age in 22 villages at smallholder farms. The sera were tested for the

presence of antibodies to T. gondii using a commercial ELISA (PrioCHECK Toxoplasma Ab

porcine) and an in-house assay (TgSAG1 p30). The overall seroprevalence based on the

commercial ELISA was 28.7% (95% CI: 25.8-31.7%). Seropositive animals were found in all

villages with significant differences across the three districts (P<0.05) and 12 sub-counties

(P<0.01) in the survey area. Cohen’s kappa statistic showed a very good level of agreement

(κ=0.7637) between the two serological assays.

Preliminary univariate analysis suggests a significant association between seropositivity and pig

age, value chain type, feeding of crop residues, source of drinking water, keeping cats on farm

compound, and frequent sightings of wildlife (especially antelopes, hares, wild and stray dogs)

near the village. The present report is the first survey documenting the seroprevalence of T. gondii

in domestic pigs in the East African Community (Burundi, Kenya, Rwanda, Tanzania and Uganda)

and investigating potential risk factors that may need attention when promoting smallholder pig

keeping as a livelihood activity in Central and Eastern Uganda. The research was carried out with

the financial support of the Federal Ministry for Economic Cooperation and Development

(BMZ/GIZ), Germany, the CRP A4NH, led by IFPRI through the SFFF project at ILRI as well as

the CRP L&F at ILRI as part of the SPVCD project.

71

Chapter 6: Knowledge, attitudes and practices of pork consumers

6 Knowledge, attitudes and practices of pork consumers (Publication V)

It is not possible to assess livestock value chains comprehensively without considering the

consumers of the principal output, in this case the meat. Not only is the consumers’ demand for

animal sourced food a main driver of livestock production, and secondly, if the edible end product

is infected with pathogens it is the consumer whose health may suffer. On the other hand, if the

consumer demands certain quality standards he or she can be critical in helping to improve the

entire value chain. We therefore wanted to find out what the attitudes of pork consumers are

towards the quality of meat and pork in particular, what they believe and know about pig and pork

zoonoses, how pork is usually prepared and how frequently it is consumed. Due to time and

financial restrictions we were not able to develop a separate sampling frame representative of all

pork consumers in the selected sites; therefore, we started by studying the knowledge, attitudes

and practices of the smallholder pig producers who are potentially pork consumers.

Tools from participatory epidemiology (PE) were used to discuss questions such as: Who eats

pork, when and why? What are reasons not to eat pork? What is the role of pork in farmers’ diets?

Are pig keepers pork eaters? How accessible is pork? Do pig feeds compete with human food?

How does knowledge, attitudes and practices increase or reduce the risk of pork-borne diseases?

Some of the key findings include that pork is widely popular among pig farmers, in rural areas

mostly during seasonal festivities and whenever cash is available, in urban areas much more

frequently. Pig keepers are pork eaters; however, they are not usually consuming their own animals

but buy pork at local (and informal) butcheries and pork joints. Reasons for not eating pork are

mainly religious and traditional beliefs, or sometimes taste preferences. According to pig farmers,

pig feed production does not compete with human food production; some festivals when pork is

consumed even coincide with times when food is not abundant. The consumption of raw pork is

considered unsafe, and at home meat is cooked for at least one hour.

Full details of the scientific findings of this chapter have been subjected to peer review and

presented as a conference paper (publication V) at the 6th All African Conference on Animal

Agriculture held in Nairobi, Kenya, from 27-30 October 2014. An author-created version of the

published article appears overleaf. The abstract is available online:

Roesel, K., Ouma, E.A., Dione, M.M., Pezo, D., Grace, D. 2016. Smallholder pig producers and

their pork consumption practices in Kamuli, Masaka and Mukono districts in Uganda. In: Africa’s

Animal Agriculture: Macro-trends and future opportunities. 6th All African Conference on Animal

Agriculture, Nairobi, Kenya, 27-30 October 2014, pages 166-168. Available online at

https://cgspace.cgiar.org/handle/10568/51344.

72

https://cgspace.cgiar.org/handle/10568/51344

Chapter 6: Publication V

73

Smallholder pig producers and their pork consumption practices in Kamuli, Masaka

and Mukono districts in Uganda

Roesel K1,2

*, Ouma EA1, Dione MM

1, Pezo D

1, and Grace D

1

1 International Livestock Research Institute,

2 Freie Universitaet Berlin

Email addresses of authors:

[email protected]*; [email protected]; [email protected]; [email protected];

[email protected]

Abstract:

Pig production is thriving in Uganda and the demand for pork is increasing, therefore offering

potential for increased income through small-scale pig production and marketing. A multi-

disciplinary value chain assessment conducted by the International Livestock Research

Institute and partners aimed to identify constraints and opportunities for value chain actors as

well as shortcomings in the safety of pork products in three districts in Uganda. Prior to

quantitative surveys and biological sampling at various nodes of the chain, participatory rural

appraisals and focus group discussions were held with about 1,400 smallholder pig farmers to

map out qualitative aspects including the various actors involved in pig rearing (e.g. input and

service providers) and marketing (e.g. marketing channels and pricing). One particular aspect

covered pork consumption habits as well as knowledge, attitudes and practices on pork safety

among 294 participants, considering that they are also food consumers. Pork is widely

popular, mostly consumed well-cooked or thoroughly pan-fried. The frequency of

consumption follows seasonal patterns and increases from rural to more urban settings.

Practices such as roasting may lead to the ingestion of undercooked pork, and accompanying

dishes such as raw vegetables may lead to cross-contamination of the meat causing foodborne

diseases. The scarcity of data on zoonotic pig pathogens, such as erysipelas, salmonellosis,

brucellosis and pork-borne parasites requires further research.

Key words: participatory research, pork safety, quality attributes, risk, women

1


74

2

Introduction:

Over the past three decades, pig numbers in Uganda have at least quadrupled (FAO, 2011;

MAAIF/UBOS, 2009) and 70% percent of the estimated 3.2 million pigs are in the hands of

smallholder farmers, many of them women (MAAIF/UBOS, 2009). Pork per capita

consumption in Uganda currently ranks highest in East Africa at 3.4 kg per year (FAO,

2011). In a consultative process, the CGIAR Research Program on Livestock & Fish (CRP

L&F), led by the International Livestock Research Institute (ILRI), has identified pigs in

Uganda as one of nine selected livestock value chains where research for development has

potential and is targeted to make an impact for poor producers and consumers (ILRI, 2011).

Until 2012, little was known about how smallholder pig value chains in Uganda operate;

where pigs come from and who eats them, constraints and opportunities in smallholder

production systems and possible public health risks associated with pig farming and pork

consumption. The present study describes knowledge, attitude, practices and perceptions

related to pork consumption and quality at the consumers’ node of the value chain.

Materials and Methods:

The present study was carried out under the Safe Food, Fair Food project which aims to

improve food safety in selected CRP L&F value chains, and was part of multidisciplinary,

multi-project activities under the umbrella of the Smallholder Pig Value Chain Development

project (SPVCD). From November 2012 to January 2013, we carried out qualitative

assessments at the producers node to map out the various actors involved in pig rearing (e.g.

input and service providers) and marketing (e.g. marketing channels and pricing) as well as to

inform in-depth and quantitative assessments and prevalence surveys that followed in 2013

(ILRI and partners, forthcoming). We carried out participatory rural appraisals, key informant

interviews and focus group discussions in 35 villages with about 1,400 smallholder pig

farmers in Masaka and Mukono districts of the Central region (436,400 pig-owning

households; MAAIF/UBOS, 2009) and Kamuli district in the Eastern region (262,300 pig-

owning households; MAAIF/UBOS, 2009) in Uganda. The farmers were engaged in

discussions on feeds, breeds, marketing, animal health, and zoonoses including food safety,

during four parallel sessions (Ouma et al, 2014).

Figure 1. The study sites Kamuli, Masaka and Mukono districts, Uganda. (ILRI/Ochungo)


75

3

In the session on food safety and nutrition, qualitative and semi-quantitative data on pork

consumption patterns, preparation methods as well knowledge, attitudes and practices on

pork safety was gathered from 294 randomly selected pig farmers (103 men and 191 women)

in 34 villages in the above mentioned districts. Generic discussion guides were used with all

groups and included tools from Participatory Epidemiology such as focus group discussions,

ranking and scoring methods, Venn diagrams and seasonal calendars. These activities were

used to answer a set of research questions, specifically: Who eats pork, when and why? What

are reasons not to eat pork? What is the role of pork in farmers’ diets? Are pig keepers pork

eaters? How accessible is pork? Do pig feeds compete with human food? How does

knowledge, attitudes and practices increase or reduce the risk of pork-borne diseases?

Table 1. Pork consumption assessment tools used by district.

Tools used PRA guide producers PRA guide

consumers

FGD with mothers

Kamuli district 4 4 5

Masaka district 14 0 14

Mukono district 6 6 8

Total 24 10 27

The data was entered into MS Excel for basic descriptive analysis and visualization.

Results: Pig producers are generally pork eaters; 80% of the pig farmers in the survey

(n=234/294) eat pork, whereas the proportion of male consumers is marginally higher (89%)

than the female (74%). Consumption is mainly driven by festivals as shown in Figure 2.

More pork is consumed when cash is available, for instance after the coffee harvest in

Masaka during June/July. Less pork is consumed at the beginning of new school terms when

pigs are sold to pay for school fees.

Figure 2. Seasonality of pork consumption among 292 pig farmers in Kamuli, Masaka and Mukono districts.

(The bars indicate proportions established by group consensus and have not been further quantified.)

Pork ranks second after chicken in terms of taste and is occasionally given to children under

five years as food for good growth. In rural sites, pork is believed to clear the skin, cure

1 2 3 4 5 6 7 8 9 10 11 12

month

Kamuli district

Masaka district

Mukono district

rainfall average all districts

Christmas

Easter Independence

Day (Kamuli only)

Martyr's Day

school fees due for payment

76


4

measles and make “strong bones” whereas in the urban areas pork is sometimes believed to

cure HIV/AIDS (Ejobi et al, forthcoming). In the rural study sites, pig farmers rarely

slaughter their own animals as they use the money generated from sales of live pigs for

meeting family needs such as school fees. The closer to urban centres, the more frequently

pork and other animal sourced food is eaten, e.g. weekly to daily, and pigs are kept for both

sale and home consumption. The biggest constraint for eating more pork in rural areas is low

income; other factors include religion or traditional beliefs. Some of the women who do not

eat pork claimed that they were raised at times when women were denied pork because men

believed that eating it makes women too strong and outspoken. Moreover, according to local

tradition in rural Masaka district, elderly women are not supposed to eat pork, chicken and

red meat. They are given eggs, fish and even bone marrow as this is believed to keep them

strong. Almost all (93%) of the mothers emphasized that nobody eats offal, referring to white

offal, partly because pigs eat anything including faeces and snakes. Farmers across all sites,

especially in rural settings, indicated they may eat meat from diseased pigs if they cannot find

a market for their animals. Food for people does not compete with pig feeds as the animals

are fed with leftovers or fattened during “times of plenty”, shortly after the seasonal rains.

The main quality criteria that pig farmers consider as important when purchasing pork are

presented in Figure 3. Cleanliness of the meat ranked first and was defined as meat free from

visible dirt and flies; a moderate fat layer (ranked second) is important because in the view of

the discussants too thick may imply human disease (e.g. high blood pressure) and too thin

could indicate pig disease (e.g. it did not gain weight because it was sick). Unbalanced

feeding of pigs was not associated with the thickness of the subcutaneous fat layer.

Figure 3. Quality attributes as perceived by pig farmers in Kamuli, Mukono and Masaka district. (The bars

indicate proportions established by group consensus and have not been further quantified.)

Raw pork is considered unsafe for human consumption and a potential source of diseases

across all sites. Pork ranked fifth after chicken, fish, beef and eggs in terms of perceived

safety; milk ranked last. All pig farmers agreed that they can contract disease from pigs;

symptoms described were worms (26%), stomach pain (20%), diarrhoea (16%) and fever

(13%). It is believed that undercooked pork can cause madness or epilepsy in humans. Fifty

percent of the participants have heard about food borne diseases in their community and 31%

rural consumer (n=23) urban consumer (n=10)


77

5

of them agreed that children are most affected. Food borne diseases are not considered fatal

but weaken the person affected and reduce his or her ability to concentrate or work. At home,

pork is thoroughly cooked for at least one hour and attempts are made to preserve the shelf-

life of raw pork, for instance by smoking and roasting. When eaten outside of the homes,

fried or roasted meat is usually consumed with raw vegetables such as tomatoes, cabbage and

onions.

People have access to pork in all study sites, and about 70% is consumed outside the homes

in pork joints. In the rural areas, consumers have less choice of butchers and the retailers are

reported to slaughter diseased animals or sell products in a dirty and unsafe environment

(Figure 4).

Figure 4. Venn diagrams developed by the group discussants to describe availability, accessibility and

preferences for sources of pork. (left: Baluboinewa village in rural Kamuli district; right: Kitete village in urban

Mukono district; the size of the circle represents the relative importance of the source)

Discussion and conclusion:

Pork is consumed widely and consumers have access to pork in all study sites but quality

seems to be neglected in the rural sites where consumers reported less sources of pork and

more meat sold from unsanitary outlets. Pork consumption on the occasion of Easter and

Christmas often coincides with times of food scarcity. A safe product can therefore contribute

to the protein supply of poor farmers and their families during seasons of food shortage.

The consumption of offal is not commonly accepted in the study sites and may need

promotion as it provides a source of protein to those who cannot afford to buy pig meat. Offal

refers to the internal organs and entrails of an animal slaughtered for meat. While the farmers

in the study sites cook red offal (heart, tongue, lungs, spleen and kidneys), white offal are

only partly used. Meat is scraped off of feet and heads, and in Masaka district bone marrow is

sometimes given to old people to help them maintain their body strength. Brains and genital

parts including the uterus and teats are not eaten at all and people do not know about the

existence of the pancreas (sweet breads) which is usually discarded in the open by the

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6

butchers together with the slaughtered animal’s stomach, intestines, blood and faeces. There

they are left for scavengers, potentially contributing to spread of diseases and environmental

pollution.

While the meat is consumed hot, the preparation of pork dishes with raw vegetables on the

side may lead to cross-contamination with foodborne pathogens. The pathognomonic signs of

diamond skin disease (Erysipelothrix rhusiopathiae) were reported in Kamuli district and

pose a risk to people handling raw pork like butchers and house wives preparing the meat.

The common misperception of the life cycle of Taenia solium causes inefficient management

of the disease risks. More research is required and currently conducted on pork parasites such

as trichinosis and both porcine and human cysticercosis due to the common practice of

roasting pork which may lead to the ingestion of parasitic larvae.

Acknowledgements:

The study was conducted under the Safe Food, Fair Food project led by the International

Livestock Research Institute and carried out with the financial support of the Federal

Ministry for Economic Cooperation and Development, Germany, and the CGIAR Research

Program on Agriculture for Nutrition and Health, led by the International Food Policy

Research Institute. We are grateful for the collaboration with and support of the Smallholder

Pig Value Chains Development Project in Uganda, financed by the European Commission

through the International Fund for Agricultural Development (IFAD) and the CGIAR

Research Program on Livestock and Fish, led by ILRI. We thank the smallholder pig farmers

who shared their views and perception on pork consumption as well as the local government

and non-governmental partners for their facilitation.

References:

Ejobi et al, 2012. Participatory Rural Appraisal with Urban Pork Consumers in Kampala,

Uganda, forthcoming.

Food and Agriculture Organization of the United Nations, Statistics Division 2011, accessed

from http://faostat3.fao.org/home/index.html#DOWNLOAD

ILRI, CIAT, ICARDA, WorldFish Center, 2011. Smallholder pig production and marketing

value chain in Uganda: Background proposals for the CGIAR Research Program on

Livestock and Fish. Nairobi, Kenya: ILRI

Ministry of Agriculture, Animal Industry and Fisheries and Uganda Bureau of Statistics,

2009. The National Livestock Census Report 2008

Ouma et al, 2014. Smallholder pig value chain assessment in Uganda: results from producer

focus group discussions and key informant interviews. ILRI (Research Report). Nairobi,

Kenya: ILRI.

Chapter 7: Summarizing discussion

7 Summarizing discussion

The aim of the present study was to contribute to the evidence base on parasitic infections in pigs

raised in smallholder production settings in Uganda. It was hypothesized that the intensification

level may affect the parasitic burden of pigs and hence potentially compromise farm productivity

and public health, whereby the value chain domain classification established by ILRI and partners

(chapter 3) served as a proxy for the level of intensification in smallholder pig value chains in

Uganda. While prevalence and potential risk factors for selected parasites have been discussed in-

depth in chapters 4 and 5, in this chapter, we will put the key findings in the overall context of

research in smallholder pig value chains in Uganda and how they contribute to the overarching

goals of the research programs led by ILRI.

7.1 Value chain domains as a suitable proxy for the classification of heterogeneous

smallholder pig production systems

Pig production in sub-Saharan Africa in general, and Uganda in particular, is increasing (see

chapter 2). The fact that numerous governments, including that of Uganda do not proactively

promote pig-keeping (Tatwangire, 2013), yet pig numbers are rising, shows that growth of this

agribusiness may be intrinsic, perhaps motivated by both the demand for pork driven by

urbanization (Robinson et al., 2014) and the preference for a livestock species that can generate

returns quickly with limited resources in the absence of access to financial infrastructure. The

various assessments of the sector and our research in Uganda show that there are many constraints

to the sector as a whole, such as poor organization and lack of governmental support, but also

particular constraints, especially to rural producers who face high disease burdens and high costs

of investments but also lack many basic skills both entrepreneurial (e.g. record keeping) and in pig

husbandry (e.g. biosecurity or pig nutrition) which makes them less competitive. But because pigs

are resilient they manage to survive under basic conditions; smallholder pig farmers could

potentially make (much more) profit if the range of knowledge gaps could be closed. While the

smallholder pig production systems in the selected study sites have been well described in chapter

4 (Dione et al., 2014) and by Ouma et al. (2014); the findings also show the heterogeneity of these

systems. All had in common that pigs are mostly kept for income generation, but important

determinants for pig health could not be categorized easily. An important example is the level of

confinement as pigs that roam and scavenge are more exposed to pathogens, yet confinement types

showed a wide variety defying rigid classification. Some farmers let pigs roam during the day and

tether or house them during the night. Others leave them roaming when fields are fallow and have

them tethered or housed during planting and harvesting season. For instance, the publication in

chapter 4 by Dione et al. (2014) showed that during the fallow season when the participatory rural

appraisals were conducted, 17.5% of the pigs were free ranging in rural production settings and

only 1% in urban production settings. A few months later, during the prevalence survey which

happened during the planting season, only a very small fraction of the pigs were free-ranging

(Roesel et al., 2017, 2016b). Yet others confine their animals if their farm is located in a

neighbourhood where pigs are not tolerated or if they have the resources to feed and house them,

which can fluctuate within a short time, for instance if the farmer experienced a poor coffee harvest

(this also illustrates the vulnerability of smallholder livestock farming systems). However, the

structured targeting process described in chapter 3 and the classification of production systems

into value chain domains offered a very suitable way to determine the level of intensification at

production and at the same time allowed to us draw conclusions on the location of the end

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consumer and therefore, the population at risk for pork-borne parasitic infection. While there was

no significant difference in gastrointestinal infection between value chain types, the serological

findings on pork-borne diseases showed that the rural population is more exposed to infection with

Trichinella spp., though our findings suggest that the risk for developing trichinellosis is very low

(Roesel et al., 2016b). Antibodies against T. gondii tachyzoite antigen on the other hand were

found at significantly higher levels in the UU settings showing increased exposure to infection of

urban butchers and consumers.

7.2 Pig parasites as a constraint to farm productivity

Gastrointestinal parasites are common in the Ugandan production systems as shown by our survey

(chapter 4) but their impact is often underestimated because infection does not cause high mortality

and may be subclinical. Losses may go unnoticed as changes in pig performance are subtle and in

small daily amounts. Studies from Western Kenya showed that average daily gains in pigs kept in

rural areas were 110 grams versus 150 grams in peri-urban pig units (Carter et al., 2013). Reasons

hypothesized were malnourishment (i.e. poor feed availability or poor rations), high energy

expenditure for maintenance (i.e. as roaming pigs expend significant calories through movement),

high parasite prevalence, other diseases, and, low genetic potential (Carter et al., 2013). The same

study reported that the average body weight at marketing age (5-10 months) was 30 kg; this is very

low compared to market weight of exotic breeds in industrialized countries (more than 90 kg at 5

months age) or 40-60 kg in rural Nigeria (Machebe et al., 2009) and 50-70 kg in periurban Nigeria

(Adesehinwa et al., 2003). Feed costs account for 70-85% of smallholders pig production costs

and given that cost and availability of pig feeds are a major production constraint, parasite control

could potentially lead to a much higher feed efficiency. Experiments have shown that growers

infected with one or more species of gastrointestinal parasites, in particular A. suum, T. suis or

Oesophagostomum spp., experienced reduced growth rates of 31-33% (Kipper et al., 2011; Stewart

et al., 1985; Hale and Stewart, 1979) as well as changed body composition, e.g. heavier plucks and

less meat (Knecht et al., 2011; Roepstorff et al., 2011). However, these studies were carried out in

industrialized countries with potentially improved breeds and in a much more controlled

environment (e.g. an otherwise balanced diet and vaccination), and there is need to repeat them in

local settings and with local breeds.

Our study showed that husbandry practices such as regular removal of faeces from pig pens or

regular cleaning and disinfection correlate with a lower parasite burden in the pig population,

which was, perhaps surprisingly, not the case for the regular use of dewormers. However, we have

to be aware that findings presented here are the results of a cross-sectional study as in previous

assessments from Uganda (Waiswa et al., 2007). From the results we are thus not able to draw

conclusions on causal relationships between exposure to a pathogen and actual infection; rather

they show statistical correlation between those two, which may be suggestive of causation. More

experimental and longitudinal studies are needed to probe findings from cross-sectional studies

and to quantify gains and losses. These could include the effect of regular deworming (including

the frequency), and of sanitary and hygiene measures as well disease incidence and mortality. A

particular focus should be given to pre-weaning and grower pigs as these are the periods of fastest

growth (Carter et al., 2013) and when morbidity and mortality seems high in the East African

smallholder production systems (Ikwap et al., 2014; Wabacha et al., 2004b). Our study (chapter 4,

publication II), too, showed an increase of gastrointestinal helminth burden from 3 to 18 months

80


(pigs younger than that were not included into the study), which then fell between 18 and 36

months of age.

7.3 Parasite infections with public health implications

7.3.1 Gastrointestinal parasites as soil-transmitted zoonotic helminths

In addition to direct performance losses, internal parasite infection in pigs, especially growers, can

generally compromise vigour and may act synergistically with other endemic potential pathogens

(Greve, 2012). In humans, gastrointestinal, or soil-transmitted helminths (STHs) are among the

most common infections worldwide and considered a neglected tropical disease by the WHO

(2016b). Infection with STHs impact the wellbeing of the infected person with disorders ranging

from general malaise and stomach pain to nutritional impairment through weight or blood loss,

diarrhoea or dysentery, loss of appetite or reduced absorption of macro- and micronutrients.

Children may experience delay in physical, intellectual, and cognitive development (Bethony et

al., 2006). In some cases, STHs cause severe complications such as intestinal obstruction or rectal

prolapse, and can be fatal if unattended. As outlined in chapter 2, A. suum and T. suis are infective

for humans (Iñiguez et al., 2012; Leles et al., 2012; Liu et al., 2012; Nissen et al., 2012; Peng and

Criscione, 2012; Zhou et al., 2012), and infection with both species has been shown to be prevalent,

especially among school children in all regions of Uganda (Brooker et al., 2009; Standley et al.,

2009; Kolaczinski et al., 2006; Kabatereine et al., 2005).

7.3.2 Pork-borne zoonoses

A long anticipated report which, for the first time, estimated the global burden attributed to

foodborne diseases, found that the overall global burden of foodborne disease (including

waterborne disease) is comparable to those of the major infectious diseases (HIV/Aids, malaria

and tuberculosis). In the African subregion that includes Uganda (Table 7.4), foodborne parasitic

diseases play a smaller role than foodborne disease caused by bacteria but a bigger role than

foodborne disease caused by viruses (Havelaar et al., 2015). The data in Table 7.4 also show that

parasitic infections cause more chronic burden than acute illness, and that T. gondii and T. solium

infections have the greatest impact. While trends are perhaps accurate, the actual burden of

foodborne diseases attributed to biological hazards may be underestimated due to a lack of

differential diagnostics and thus lack of attribution data in low-income countries. Also, the

presence of parasitic diseases in food producing animals such as pigs is still underresearched in

sub-Saharan Africa (Alonso et al., 2016).

Of all the pork-borne parasites, “the three T” parasites have been responsible for most pork-borne

illness throughout history (Djurković-Djaković et al., 2013). While the research presented in

chapter 5 investigated the occurrence of infection with Trichinella and Toxoplasma gondii, the

“third T”, Taenia solium, was researched in the same cohort by a different scientist in the team. A

comparative literature analysis on the disease situation and predisposing factors in selected

countries including Uganda showed that there is limited knowledge on life cycle of the tapeworm

by key players including farmers, butchers, veterinary staff and consumers; poor husbandry and

sanitation practices contributing to the maintenance of the life cycle are very common; and that

prevalence data on porcine infection is scanty and reports on human infection levels are very scarce

(Kungu et al., 2015). A prevalence survey in the same pig cohort subject in chapters 4 and 5

showed lower levels of infection with T. solium in rural production settings (10.8%) than in urban

81


settings (17.1%) (Kungu et al., 2016). This was also true for pig infections with T. gondii but the

opposite case for infections with Trichinella spp.

FAO recommends the daily per capita consumption of 20 g animal protein per person (7.3 kg per

person per year) (FAO, 2015); the average daily protein intake in Uganda was 12.38 g from animal

sourced foods including milk, meat, eggs, fish, and offal (FAOSTAT, 2011), hence moderate pig

meat consumption could contribute to improved nutrition security. Some examples presented in

detail in chapters 4-6 show how smallholder farmers do indeed consume pork but only

occasionally, especially during festivals such as Christmas, but the frequency of consumption

increases towards more urban settings to an average of twice a week in Kampala (chapter 6 and

Heilmann et al., 2016). Only 10% of the pig producers practice home slaughter (chapters 5 and 6),

which is lower than the 33% in rural Western Kenya (Githigia et al., 2005), and most pigs are sold

for consumption in urban centres (RU, UU value chains) or local rural eateries (RR value chain),

often via middlemen. It is worrying that there is little or no meat inspection, a scenario similar to

rural Western Kenya (Githigia et al., 2005), and a characteristic trait of informal markets in low-

income countries. In the whole of Uganda, there is only one formally recognized pig abattoir where

meat inspectors are employed but a descriptive survey showed that inspection is not structured,

solely based on macroscopic lesions (e.g. Cysticercus cellulosae), and not risk-based. Pigs are not

traceable, data on diseases prevalent in the production areas is lacking and neither laboratory

diagnostics nor condemnation policies are enforced (Roesel et al., 2016a). On the other hand, raw

pork consumption is not commonly practiced and pork, if prepared and consumed at home, is

cooked for a long time (chapter 6) likely to kill parasitic stages in the meat. However, infection

with infectious parasitic stages in pork (e.g. ruptured cysts with T. gondii bradyzoites) may occur

during pork handling (occupational disease). In addition, methods such as roasting that are more

common at pork joints may lead to the ingestion of undercooked pork, and accompanying dishes

such as raw vegetables may lead to cross-contamination of the meat causing foodborne diseases

(Heilmann et al., 2016, 2015).

Across all sites, raw pork is generally considered unsafe for human consumption and is seen as a

potential source of disease (chapter 6); health aspects associated with visible meat quality (e.g.

cleanliness, colour or fat layer) are important to the pork-consumers in this study and have been

confirmed to be important criteria influencing the buying decision of urban pork consumers in

Kampala (Heilmann et al., 2016). As most pork is produced by rural farmers and consumed by

urban dwellers, organizing and educating urban consumers instead of trivializing (Figures 7.1 and

7.2), paired with increased income in the cities could potentially stimulate greater demand not only

for quantity but also for quality of meat products (Adesehinwa et al., 2003).

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Table 7.1 The median global numbers of foodborne illnesses, deaths and Disability Adjusted Life Years (DALYs) compared to the median rates of DALYs in the African sub-

region E (AFR E) which includes Uganda. Source: Havelaar et al. (2015).

Hazard Foodborne illness,

global (%)

Foodborne deaths,

global (%)

Foodborne DALYs8, global (%) Foodborne DALYs,

AFR E9 (%)

Protozoa 75,124,588 (13.08) 5,913 (1.49) 1,290,360 (4.11) 37,700 (3.45)

Cryptosporidium spp. 8,584,805 (1.50) 3,759 (0.95) 296,156 (0.94) 1,200 (0.11)

Entamoeba histiolytica 28,023,571 (4.88) 1,470 (0.37) 138,863 (0.44) 5,000 (0.46)

Giardia spp. 28,236,123 (4.92) - 26,270 (0.08) 700 (0.06)

Toxoplasma gondii10 10,280,089 (1.79) 684 (0.17) 829,071 (2.64) 20,000 (1.83)

Helminths 12,924,132 (2.25) 44,897 (11.31) 5,752,017 (18.31) 181,819 (16.62)

Echinococcus granulosus 43,076 (0.01) 482 (0.12) 39,950 (0.13) 800 (0.07)

Echinococcus multilocularis 8,375 (<0.01) 7,771 (1.96) 312,461 (0.99) -

Taenia solium 370,710 (0.06) 28,114 (7.08) 2,788,426 (8.87) 176,000 (16.08)

Ascaris spp. 12,280,767 (2.14) 1,008 (0.25) 605,278 (1.93) 5,000 (0.46)

Trichinella spp. 4,472 (<0.01) 4 (<0.01) 550 (<0.01) 1 (<0.01)

Clonorchis sinensis 31,620 (0.01) 5,770 (1.45) 522,863 (1.66) -

Fasciola spp. 10,635 (<0.01) - 90,041 (0.29) 10 (<0.01)

Intestinal flukes11 18,924 (<0.01) - 155,165 (0.49) -

Opisthorchis spp. 16,315 (<0.01) 1,498 (0.38) 188,346 (0.60) -

Paragonimus spp. 139,238 (<0.02) 250 (0.06) 1,048,937 (3.34) 8 (<0.01)

Bacteria 347,415,818 (60.50) 263,925 (66.47) 19,632,153 (62.48) 785,380 (71.77)

Viruses 138,513,782 (24.12) 62,660 (15.78) 3,849,845 (12.25) 94,000 (8.59)

Chemicals and toxins 216,270 (0.04) 19,682 (4.96) 895,128 (2.85) 6,200 (0.57)

Total: 574,194,590 (100.00) 397,077 (100.0) 31,419,503 (100.00) 1,094,299 (100.00)

8 Disability Adjusted Life Years (DALYs) are used as a measure of population health and combine the years of life lost due to premature death and the years lived with disability from a disease or

condition, for varying degrees of severity (Murray and Lopez, 1997) 9 Subregion AFR E: Botswana; Burundi; Central African Republic; Congo; Côte d'Ivoire; Democratic Republic of the Congo; Eritrea; Ethiopia; Kenya; Lesotho; Malawi; Mozambique; Namibia;

Rwanda; South Africa; Swaziland; Uganda; United Republic of Tanzania; Zambia; Zimbabwe. The term subregion does not refer to the WHO member states, it combines the geographical region child

and adult mortality levels as described by Ezzati et al. (2002) 10 Numbers presented here refer to the burden of congenital toxoplasmosis 11 Includes families Echinostomatidae, Fasciolidae, Gymnophallidae, Heterophyidae, Nanophyetidae, Neodiplostomidae and Plagiorchiidae


83


Figure 7.1 An article published by the newspaper Uganda

Daily Monitor on 6 June 2012 referring to a report that

suggests high contamination of pork in Kampala. On

inquiry, the Kampala City Council Authority's (KCCA)

senior veterinary officer explained that there is no report.

Statements on pork safety were based on misperceptions not

evidence. Source: Safe Food, Fair Food blog post (ILRI,

2012c).

Figure 7.2 One week later, on 13 June 2016, the Ugandan

populist newspaper Red Pepper declared a war on informal

pork butcheries operating in Kampala, referring to the same

misleading “expert report”. Source: Safe Food, Fair Food

blog post (ILRI, 2012c).

Improving pig husbandry practices on farm has emerged as a critical factor for (zoonotic) disease

control from various sub-activities in the program (Roesel et al., 2017; Dione et al., 2015a; Kungu

et al., 2015), and many good hygiene practices have been shown to be successful and well-

documented in other countries, for instance by FAO (2010). Knowing what works best is vital for

improving smallholder production systems; however, implementation of best-practices (e.g.

housing to prevent exposure to zoonotic pathogens) requires initial financial resources that the

smallholder farmer will have to bear. But currently, pig-keeping is particularly attractive to

resource-poor smallholders (Lekule and Kyvsgaard, 2003; Phiri et al., 2003; Verhulst, 1993) who

will not have the means to adapt technology or practice unless they are given incentives, for

instance if consumers are willing to pay a premium for higher quality which reaches the producer.

On the other hand, many practices have been known to contribute towards the control of a problem,

for instance T. solium, and the use of latrines has been promoted for decades. However, open

defecation is not only linked to the physical access of water or latrines; a recent study conducted

by Thys et al. in Zambia (2015) showed that although latrines were perceived to contribute to good

hygiene, because they prevent pigs from eating human faeces. Nonetheless people (especially

men) expressed reluctance to abandon the practice of open defecation due to cultural taboos. These

are especially found in matrilineal cultures such as the Bantu people, who also dominate large parts

of Uganda.

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7.4 Researching smallholder pig value chains through an integrated approach and

participatory methods

Mbuthia et al. (2015) acknowledged that for smallholder pig farming improvement programmes

to be successful, there is the need for appropriate understanding of these systems so as to

holistically address their constraints. In the Ugandan smallholder pig value chains, the CRPs have

been the first to also include nodes to their assessments that were not only linked to inputs

increasing farm productivity (feeds, drugs) but also the value chain system at post-harvest (market

access, butchers, consumers) (Figure 7.3 and Ouma et al., 2014). The multi-pathogen prevalence

survey, of which the parasitic assessment was one component, has provided information on pig

pathogens that have never been documented from Uganda before (e.g. Brucella suis,

Erysipelothrix rhusiopathiae, Trichinella spp., T. gondii, Yersinia enterocolitica), and pathogens

known to be present in Uganda (e.g. African swine fever virus, Taenia solium). Moreover, testing

for more parasites (e.g. Sarcoptes scabiei var. suis, Trypanosoma spp.) as well as bacterial and

viral pathogens in the same cohort of pigs is still in progress. Joint resources from two CRPs

allowed collection of data from a big cohort, which increases statistical power of the results and in

the future will facilitate more analysis from the sample, for instance on multimorbidity or intra-

cluster correlation. These data will support scientists in designing follow up studies and target

limited resources for research.

Participatory methods have proven useful in identifying priority constraints to pig health in

smallholder production systems, and in describing production systems and husbandry practices as

well as in scoping diseases that present with clinical signs and can be seen macroscopically. These

include specific gastrointestinal worms, ectoparasites or diseases that present with pathognomonic

signs. For example, in Kamuli district, farmers reported the diamond-shaped skin lesions in their

pigs that are characteristic for acute swine erysipelas caused by Erysipelas rhusiopathiae (chapter

6). The pathogen was not on the initial list to investigate but its presence has then been confirmed

in the laboratory, showing a high level of infection among animals, meat and raw pork handlers

(Musewa, 2016). For other conditions such as disease syndromes, symptoms such as fever,

diarrhoea, and vomiting can be described, however, a conclusive etiologic diagnosis cannot be

made and findings have to be interpreted with care and supported by laboratory findings. This is

the case for ASF which has been identified a priority disease among farmers, yet in their pigs they

are only able to observe signs such as haemorrhage, fever, shivering, huddling, and sudden death

which are commonly seen in other diseases such as classical swine fever, salmonellosis, erysipelas,

infections with T. simiae among others. In the pig cohort for which laboratory results are presented

here, no antibodies to ASF were detected using INGENASIA protocols; however, one animal

tested positive for virus antigen using real time PCR (Akol et al., 2015).

Infections that are usually asymptomatic in pigs, for instance with T. solium, Trichinella spp. or T.

gondii, cannot be observed by the farmer and will therefore not be mentioned in participatory

epidemiology exercises. Nevertheless, through participatory methods we are able to get indications

on good and poor practices at production, processing and consumption level that allow better

targeting of resources towards in-depth assessments or interventions; these include husbandry

practices on farm, preparation of meat, frequency of consumption, modes of pork preparation and

knowledge on zoonotic pig diseases in smallholder pig farming communities. The use of Venn

Diagrams illustrated sources of pork, their distance from the homesteads and quality attributes that

are important to smallholder pig producers outside of the big urban centres (chapter 6, Figure 4).

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86

Figure 7.3 Synthesized results of the Ugandan smallholder pig value chain assessment including porcine parasites. The work was presented by the author at Tropentag conference

in Prague, September 2014. Source: Ouma et al. (2014).


Participatory methods can indeed be a helpful tool in assessing exposure to food safety risks in

informal markets of low-income countries as described earlier (Roesel et al., 2014).

Feedback workshops, where the scientific findings of each sub-activity were discussed with the

value chain stakeholders, have been held since the program’s inception (chapter 3), and are not

only inclusive but help communicating evidence-based findings and solutions in a more bottom-

up approach. Based on the assessment findings, seven training modules including parasite control

were developed and are tested and validated in the field with smallholder pig producers (Dione et

al., 2015b), existing materials have been updated for use in the local setting in Uganda (ILRI and

Medical Research Council, 2005), and researchers have been invited to present findings at pig

farmer trainings organized by the private sector (ILRI, 2014a). Moreover, training workshops have

been held with different stakeholders at the various nodes of the pig value chain, i.e. veterinary

public health (ILRI, 2014b). The downside of the intensive interaction with all stakeholders

through the application of participatory methods is the increased pressure on scientists to

compensate for the big gap in public veterinary extension systems by not only generating data and

developing intervention strategies but to implement them at large scale with research resources.

7.5 Concluding remarks, limitations of the survey and potential future research

The present study was able to contribute to the increasing evidence base on prevalent pig parasites

that may compromise farm productivity but also pork safety in smallholder pig production settings

in Uganda.

7.5.1 Some of the major research findings are presented below:

Results from participatory rural appraisals show that pig keeping systems are dominated

by tethering and scavenging in rural areas, while in peri-urban and urban areas,

confinement in pens is more common. High disease burden, poor housing, poor feeding,

poor veterinary services, ineffective drugs and a general lack of knowledge on piggery

management were identified as the main production constraints by smallholder pig farmers.

Second only to ASF, parasites, especially gastrointestinal worms and sarcoptic mange,

were perceived to contribute largely to market losses due to stunting across all value chain

domains and study sites.

The majority (61.4%) of all pigs were found to be infected with at least one species of

gastrointestinal helminths: 57.1% strongyle species, 7.6% Metastrongylus spp., 5.9% A.

suum, 4.2% Strongyloides ransomi, and 3.4% Trichuris suis. There were no statistically

significant differences across the different value chain types but across the different study

districts. Infection with A. suum and Metastrongylus spp. were significantly more common

in rural Kamuli districts (p < 0.01) than in the other two districts while S. ransomi was

more commonly found in urban Mukono district (p < 0.01). Coccidia oocysts were found

in 40.7% of the sampled pigs, with significantly higher levels in the more urban Mukono

district. None of the animals showed infection with Balantidium coli or Fasciola hepatica.

A logistic regression model showed that routine management factors had a greater impact

on the prevalence of infection than regular treatment or the level of confinement. Factors

negatively correlating with gastrointestinal helminth infection were routine manure

removal, and the routine use of disinfectants.

87


The overall prevalence of Trichinella-specific antibodies was 6.9% out of 1,125 sampled

animals but showed significantly higher levels in value chain types with a rural origin of

production (RR and RU value chains) (p < 0.05). Kamuli district, where the RR value chain

type dominates showed a significantly higher ELISA-prevalence than the more urban

Masaka and Mukono districts (p < 0.001). For the first time, a study in pigs in sub-Saharan

Africa was able to confirm 31 % ELISA-positive samples by Western Blot. Isolation of

infective first-stage larvae from 499 samples in ELISA clusters to identify the dominating

Trichinella spp. was not successful.

Toxoplasma-specific antibodies were found in 28.7% of the animals using a commercial

ELISA kit; village herd prevalence was 100%. Pigs raised in urban production settings (UU

value chain types) showed significantly higher levels of seropositivity than animals of a

rural production origin (RR and RU value chain types) (p < 0.007); and significantly higher

levels were shown for Masaka and Mukono compared to rural Kamuli district (p > 0.05).

Moreover, univariate analysis suggested a significant association between seropositivity

and pig age, feeding of crop residues, source of drinking water, keeping cats on farm

compound, and frequent sightings of wildlife (especially antelopes, hares, wild and stray

dogs) near the village. The present report is the first survey documenting the seroprevalence

of T. gondii in domestic pigs in the East African Community.

Findings on pork consumption practices from participatory rural appraisals showed that

pork is widely popular among pig farmers. In rural areas it is consumed mostly during

seasonal festivities and whenever cash is available, in urban areas much more frequently.

According to the pig farmers, pig feed production does not compete with human food

production; some festivals when pork is consumed even coincide with times when other

food is not abundant. The consumption of raw pork is considered unsafe, and at home meat

is cooked for at least one hour.

7.5.2 Major conclusions that can be drawn from this assessment are:

Smallholder pig production systems in Uganda are highly heterogeneous and complex, and

the level of intensification cannot be characterized by a single variable such as the level of

confinement. Due to the informal setting of the pig sector, even a fully confined pig may

be exposed to parasites introduced to the farm, e.g. feeds contaminated with rodents or cat

faeces. Using a proxy of value chain domains that comprised different aspects, in this case

pig population density, poverty levels and the time to reach the nearest market, was useful

for comparing pig populations in different villages.

Infections with gastrointestinal parasites are common but weight loss, a consequence of

worm infection as perceived by pig farmers, could not be attributed to a particular parasite

species. Other factors causing malnutrition due to poor pig diets, or potentially a

combination of these two, have not been investigated in this cohort of pigs. Regular

treatment with anthelminthics alone is not useful in containing the burden of infection at

acceptable levels if efficient hygiene farming practices such as regular removal of faeces,

cleaning and disinfection of pig pens are not followed.

88


The Trichinella species infecting domestic pigs needs to be identified by isolation of

muscle larvae, which was not successful in this study. Subsequently, serological assays

developed for the diagnostics of Trichinella infection in domestic pigs in high-income

countries need to be adapted for use in the local settings of smallholder pig production in

the tropics.

The findings on the seroprevalence of antibodies to T. gondii in domestic pigs imply that

more research should be carried out to determine the genotype infecting pigs as well as the

tissue cyst burden to be able to re-assess the risk for human raw pork handlers and the

vulnerable population, e.g. pregnant women and HIV/Aids patients. Consequently, in-

depth research on transmission routes for domestic pigs and humans is warranted.

The high prevalence of gastrointestinal parasites, some of them zoonotic, may expose pig

farmers and their children, who often tend to the pigs, to disease. While, according to the

findings of this study, the risk for developing trichinellosis is low, the risk for infection

with T. gondii from raw pork handling or other practices on farm (e.g. handling feeds, or

drinking contaminated with oocysts) is higher.

Constraints to the parasitic assessment were mostly related to the design of the overall pig value

chain assessment which was cross-sectional and could therefore suggest but not prove causal

relationships between exposing variables and parasite infection. Despite the outweighing benefits

described above, a shortcoming of the prevalence survey for parasitic assessment, was the

exclusion of pigs younger than three months from the sample population as this is the age when

they are most susceptible to infection with gastrointestinal parasites. Moreover, the tight field

sampling schedule and limited time, space and human resources did not allow for the collection

and analysis of urine to determine the prevalence of Stephanurus dentatus (kidney worm), to

perform larval culture and coccidia oocyst sporulation, or to collect deep skin scrapings and

ectoparasites from all pigs, which could have added useful information. Specimens were collected

from a number of pigs but this was not done systematically.

Additional laboratory experiments conducted after the prevalence survey included artificial

digestion to potentially isolate first-stage larvae of Trichinella spp. clusters and a mouse bioassay

to isolate T. gondii bradyzoites for genotyping in ELISA clusters. While the sample for the

artificial digestion was large (n=499), no larvae could be isolated and reasons were exhaustively

discussed in chapter 5. However, the serological status of the digested samples could not be

confirmed due to limited resources. Attempts to isolate T. gondii in a mouse bioassay were also

not successful, even though only serologically positive samples had been used as recommended

(Dubey, 2009). T. gondii bioassays in cats have been shown to be more successful in the isolation

of viable cysts as larger volumes (500g) or more can be assayed than in mice; however, facilities

for experiments involving cats were not available in Uganda at the time of the study.

Future research on pig parasites in Uganda should aim at:

Quantifying actual losses due to gastrointestinal parasites on farm by means of

experimental studies and longitudinal surveys;

89


Characterizing pork pathogens, for instance the Trichinella species infecting pigs in

Uganda or the genotype involved in porcine infection with T. gondii;

Assessing the effect of co-infection on the sensitivity and specificity of serological assays

developed and validated in high-income countries;

Quantifying the risk for pork-borne parasitic diseases to consumers through experimental

studies and quantitative risk assessments;

Assessing host preferences of biting insects such as tsetse flies including pigs;

Assessing the role of Ugandan pigs as potential reservoir or amplifying host for zoonotic

arboviruses such as Ndumu transmitted by Culicoides spp. (Masembe et al., 2012); Zika

virus transmitted by Aedes spp. (Chan et al., 2016), or Japanese encephalitis transmitted by

Culex spp. (Mellor and Leake, 2000);

Characterizing African pig breeds and their genetic tolerance or susceptibility to parasitic

diseases as has been shown for African cattle (Gifford-Gonzalez and Hanotte, 2011);

Including wild Suidae in parasitic assessments as they could potentially share vector-borne

infections such as with B. trautmanni (Penzhorn, 2006), or trypanosomes (Mehlitz, 1987;

Mwambu and Woodford, 1972; Van Den Berghe and Zaghi, 1963);

Investigating the role of potential hosts such as dogs and rodents as mechanical vectors

(e.g. T. gondii, A. suum), or definite hosts (e.g. Trichinella spp., Echinococcus spp.,

Neospora caninum, Sarcocystis spp.) for potentially pig-mediated zoonoses in low-income

countries, where they are often stray;

Testing the feasibility of dogs or chickens as bio-indicators and sentinels for infections

with T. gondii (Ayinmode and Jones-Akinbobola, 2015; Davoust et al., 2015; Salb et al.,

2008; Meireles et al., 2004)

90

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107

Summary

Summary

The surging demand for pork in Uganda provides an opportunity to set poor farmers on pathways

out of poverty by increasing production and market access. At the same time, markets have become

more complex and threaten the continuous presence of smallholder farmers: pig diseases and other

factors hinder a constant supply while foodborne diseases may impair the quality and safety of the

farmers’ products. The intensification level may affect the parasitic burden of pigs and hence the

profitability of pig farming as well as the risk to human health associated with pork borne parasites.

Research on parasitic hazards in smallholder pig value chains in Uganda has so far been limited,

and therefore, the present study aims, as described in chapter 1, to contribute to improving selected

smallholder pig value chains in Uganda by increasing the evidence base on prevalent parasitic

diseases.

Chapter 2 outlines the history of pigs in Africa, describes the current smallholder pig production

systems in sub-Saharan Africa, and reviews the current state of knowledge on parasitic pig diseases

compromising farm productivity as well as parasitic diseases that are potentially transmitted to

humans through pork consumption or for which pigs are known to be a natural disease reservoir.

The review refers to previous research from sub-Saharan Africa, and particularly Uganda.

Chapter 3 describes the context of the study and how it fits into overarching research for

development on smallholder pig value chains in Uganda led by the International Livestock

Research Institute (ILRI). It further describes how 35 villages were selected to be included into

the survey, how value chain systems were defined as a proxy for the level of intensification, and

characteristics of the area under study.

Chapter 4 shows that both endo- and ectoparasites are perceived as an important production

constraint by smallholder pig farmers in Central and Eastern Uganda, second only to African swine

fever. Herd dynamics and husbandry practices in the predominating production settings were

established by means of participatory rural appraisals with 340 smallholder pig farmers in the

selected sites. Consecutively, a cross-sectional parasitological study in 21 of the 35 selected

villages established baseline information on the rate and determinants of infection with

gastrointestinal helminths and coccidia in 932 randomly sampled pigs between 3 to 36 months of

age. The majority of pigs (61.4%; 95% confidence interval [CI]: 58.2-64.5%) tested positive for

one or more gastrointestinal helminths, namely strongyles (57.1%; 95% CI: 53.8-60.3%),

Metastrongylus spp. (7.6%; 95% CI: 6.1-9.6%), Ascaris suum (5.9%; 95% CI: 4.5-7.6%),

Strongyloides ransomi (4.2%; 95% CI: 3.1-5.7%) and Trichuris suis (3.4%; 95% CI: 2.4-4.8%).

Coccidia oocysts were found in 40.7% of all pigs sampled (95% CI: 37.5-44.0%). All animals

tested negative for Fasciola spp. and Balantidium coli. There were no statistically significant

differences in prevalence across value chain domains, and regression analysis showed that routine

management factors had a greater impact on the prevalence of infection than regular preventive

medical treatment or the level of confinement.

Chapter 5 provides baseline information on two pork borne zoonoses of global importance, namely

infection with Trichinella spp. and Toxoplasma gondii, in the same cohort of pigs. Trichinella-

specific immunoglobulin G was found in 6.9% of the animals (95% CI: 5.6-8.6%) using a

commercially available enzyme-linked immunosorbent assay (ELISA). Confirmatory testing by

Western blot implied an overall seroprevalence of 2.1% (95% CI: 1.4-3.2%), and attempts to

isolate muscle larvae using artificial digestion were unsuccessful. Implications for diagnostics

108

Summary

were discussed and the risk to pork consumers for developing trichinellosis was classified as low.

Antibodies to T. gondii were found in 28.7% of the animals (95% CI: 25.8-31.7%) at significantly

higher levels in urban areas of production and consumption, and risk factors that potentially

contribute to infection (e.g. biosecurity practices and access to cats) were identified.

Chapter 6 outlines the findings on common preparation and consumption practices as well as

sources of pork for consumption in the study area. These show that pork is very popular among

pig farmers. In rural areas it is consumed mostly during seasonal festivities and whenever cash is

available, in urban areas much more frequently. Pig feed production does not compete with human

food production, and some festivals when pork is consumed even coincide with times when other

food is scarce. The consumption of raw pork is considered unsafe, and at home meat is cooked for

at least one hour.

Chapter 7 discusses the findings, conclusions and limitations of the overall study and generates

recommendations for potential interventions and further research. Parasitic infections in

smallholder pig value chains in Uganda are common; and while no significant difference was

observed in overall infection rates with gastrointestinal helminths, specific parasites were detected

at significantly higher levels in urban (e.g. T. gondii) or rural value chain types (e.g. Trichinella

spp.). Further in-depth research is needed to identify the circulating Trichinella spp. and T. gondii

genotype, as well as more experimental and longitudinal studies to quantify economic losses of

parasite infection, and to establish predominant transmission routes and thus control points for

parasite control.

109

Zusammenfassung

Zusammenfassung

Untersuchungen zu parasitären Infektionen, inklusive ausgewählter Zoonosen, in

Hausschweinepopulationen in kleinbäuerlichen Wertschöpfungsketten in Uganda

Die steigende Nachfrage nach Schweinefleisch in Uganda bietet ressourcenschwachen

Kleinbauern einen Ausweg aus ihrer Armut, sollte es ihnen gelingen, Schweine rentabel zu halten

und zu vermarkten. Gleichzeitig werden diese Märkte immer komplexer und erhöhen den Druck

auf kleinbäuerliche Schweinehalter: Infektionskrankheiten und andere Faktoren bedrohen eine

konstante Versorgung des Marktes, und zoonotische Erreger beinträchtigen gegebenenfalls die

Qualität und Sicherheit des Endproduktes. Der Intensivierungsgrad bedingt möglicherweise das

Ausmaß der Infektion mit Parasitosen und somit die Wirtschaftlichkeit der Schweinehaltung und

das Risiko für den Verbraucher. Es gibt nur wenige Untersuchungen zu Parasitosen in

kleinbäuerlichen Schweinebetrieben in Uganda, und die vorliegende Arbeit hat zum Ziel, wie in

Kapitel 1 beschrieben, einige dieser Kenntnislücken schließen zu helfen.

Kapitel 2 skizziert die Geschichte des Hausschweins in Afrika, beschreibt die derzeitigen

kleinbäuerlichen Schweinehaltungssysteme im Afrika südlich der Sahara und bespricht den

aktuellen Wissensstand zu wirtschaftlich relevanten Schweineparasitosen als auch zoonotischen

Erkrankungen, die über den Fleischverzehr übertragen werden oder für die Schweine natürliches

Reservoir sind. Die Literaturrecherche bezieht sich besonders auf den Sachstand in Subsahara-

Afrika und hier ganz besonders Uganda.

Kapitel 3 beschreibt den Kontext der Studie und ordnet sie in ein umfassendes Programm des

International Livestock Research Instituts (ILRI) ein, das durch „Forschung für Entwicklung“ mit

der Optimierung kleinbäuerlicher Nutztierwertschöpfungsketten zur Armutsbekämpfung

beizutragen versucht. Das Kapitel erläutert ferner, wie die 35 Studienorte ausgewählt,

Wertschöpfungsketten stellvertretend für den Intensivierungsgrad definiert wurden und faßt

Charakteristika der Studienstandorte zusammen.

Kapitel 4 zeigt, dass Endo- und Ektoparasiten als bedeutendes Produktionshemmnis von

kleinbäuerlichen Schweinehaltern in Zentral- und Ost-Uganda wahrgenommen werden;

Parasitosen stehen an zweiter Stelle nach der Afrikanischen Schweinepest. Herdendynamik und

Haltungsbedingungen wurden mittels partizipativer Methoden mit 340 Schweinehaltern

beschrieben und teils quantifiziert. Danach wurde in 21 der 35 Studienstandorte eine

Querschnittsstudie durchgeführt, die in einer Stichprobe von 932 Tieren im Alter zwischen 3 und

36 Monaten Daten zu Infektionsrate und korrelierenden Faktoren mit gastrointestinalen

Helminthen und Kokzidien erhob. Die Mehrheit der Schweine (61.4%; 95% Konfidenzintervall

[KI]: 58.2-64.5%) war mit mindestens einer Helminthenart infiziert, hauptsächlich Magen-Darm-

Strongyliden (57.1%; 95% KI: 53.8-60.3%), Metastrongylus spp. (7.6%; 95% KI: 6.1-9.6%),

Ascaris suum (5.9%; 95% KI: 4.5-7.6%), Strongyloides ransomi (4.2%; 95% KI: 3.1-5.7%) und

Trichuris suis (3.4%; 95% KI: 2.4-4.8%). Kokzidienoozysten wurden in 40.7% aller Tiere

diagnostiziert (95% KI: 37.5-44.0%) und der Befund für Infektionen mit Fasciola spp. und

Balantidium coli war in allen Tieren negativ. Es gab keine statistisch signifikanten Unterschiede

in der Prävalenz zwischen den verschieden Typen der Wertschöpfungsketten und eine

Regressionsanalyse zeigte, dass routinemäßig ausgeführte Hygienepraktiken einen größeren

Einfluss auf die Prävalenz hatten als regelmäßige medikamentöse Prophylaxe oder Aufstallung.

110

Zusammenfassung

Kapitel 5 präsentiert Basisdaten in der gleichen Kohorte von Tieren zu zwei weltweit

vorkommenden Zoonosen, die durch den Verzehr von Schweinefleisch übertragen werden

können: Trichinella spp. und Toxoplasma gondii. Trichinella-spezifisches Immunglobulin G

wurde mittels kommerziellem ELISA in 6.9% der Tiere detektiert (95% KI: 5.6-8.6%,). Nach

Durchführung eines Western Blot zur Bestätigung sank die Seroprävalenz auf 2.1% (95% KI: 1.4-

3.2%,). Der Versuch, infektiöse Larven mithilfe der Verdaumethode zu isolieren, blieb erfolglos.

Schlussfolgerungen für die Diagnostik wurden diskutiert und das Risiko des Verbrauchers, durch

den Verzehr von Schweinefleisch klinische Trichinellose zu entwickeln, wurde als gering

eingestuft. Spezifische Antikörper gegen T. gondii wurden in 28.7% der Tiere festgestellt (95%

KI: 25.8-31.7%,), das Infektionsniveau war signifikant höher in urbanen Produktions- und

Verzehrsgebieten. Faktoren, die mit einer Infektion korrelierten, waren Hygienepraktiken und der

Zugang von Schweinen zu Katzen.

Kapitel 6 stellt die Ergebnisse einer Studie zu den Verzehrsgewohnheiten von Schweinefleisch

unter den kleinbäuerlichen Produzenten vor. Schweinefleisch ist sehr beliebt, und während es in

ländlichen Gebieten eher unregelmäßig konsumiert wird, z.B. an besonderen Anlässen oder wenn

die Familie genug Geld zur Verfügung hat, nimmt der Verbraucher im Städtischen viel häufiger

Schweinefleisch zu sich. Die Bereitstellung von Schweinefutter konkurriert nicht mit

Lebensmitteln für den menschlichen Verzehr, manche Festlichkeiten, an denen Schweinefleisch

gegessen wird, fallen sogar in Zeiten, in denen das Nahrungsmittelangebot knapp ist. Der Verzehr

von rohem Fleisch wird als nicht sicher angesehen und Schweinefleisch für den Verzehr zu Hause

mindestens eine Stunde erhitzt.

Kapitel 7 diskutiert die Ergebnisse und Schlussfolgerungen der vorangegangenen Kapitel,

Grenzen der vorgelegten Arbeit und Möglichkeiten für künftige Interventionen und

Untersuchungen. Parasitäre Infektionen in kleinbäuerlich gehaltenen Schweinen in Uganda sind

weit verbreitet. Während es zwischen Infektionsraten mit gastrointenstinalen Helminthen keine

statistisch signifikanten Unterschiede zwischen den verschiedenen Wertschöpfungskettentypen

gab, war die Infektionsrate mit T. gondii signifikant höher in urbanen Produktionssystemen und

das Vorkommen von Trichinella spp. Antikörper signifikant höher in ländlichen Gebieten.

Tiefergehende Studien zur Bestimmung der zirkulierenden Trichinella-Spezies und T.-gondii-

Genotypen sind nötig, ebenso wie experimentelle und Langzeitstudien, um wirtschaftliche

Verluste zu quantifizieren und Übertragungswege und Kritische Kontrollpunkte für Parasitosen zu

identifizieren.

111

Publications

List of own publications

The following section lists the author’s publications during the period of the study.

1. Peer-reviewed journal publications

Kungu, J.M., Dione, M., Roesel, K., Ejobi, F., Ocaido, M. and Grace, D. 2017. Assessment of

hygiene practices of pork retail outlets in Kampala district, Uganda. International Food

Research Journal 24(4): 1368–1373. http://www.ifrj.upm.edu.my/ifrj-2017-24-issue-4.html

Heilmann, M., Roesel, K., Grace, D., Bauer, B. and Clausen, P.-H. 2017. The impact of

insecticide treated material to reduce flies among pork outlets in Kampala, Uganda.

Parasitology Research 116(6):1617-1626. http://dx.doi.org/10.1007/s00436-017-5450-x

Roesel, K., Nöckler, K., Baumann, M.P.O., Fries, R., Dione, M.M., Clausen, P.-H. and Grace,

D. 2016. First report of the occurrence of Trichinella-specific antibodies in domestic pigs in

Central and Eastern Uganda. PLOS ONE 11(11): e0166258.

http://dx.doi.org/10.1371/journal.pone.0166258

Roesel, K., Dohoo, I., Baumann, M., Dione, M., Grace, D. and Clausen, P.-H. 2016.

Prevalence and risk factors for gastrointestinal parasites in small-scale pig enterprises in

Central and Eastern Uganda. Parasitology Research http://dx.doi.org/10.1007/s00436-016-

5296-7

Alonso, S., Lindahl, J., Roesel, K., Traoré, S.G., Yobouet, B.A., Ndour, A.P.N., Carron, M.

and Grace, D. 2016. Where literature is scarce: observations and lessons learnt from four

systematic reviews of zoonoses in African countries. Animal Health Research Reviews

17(01): 28–38. http://dx.doi.org/10.1017/S1466252316000104

Erume, J., Roesel, K., Dione, M.M., Ejobi, F., Mboowa, G., Kungu, J.M., Akol, J., Pezo, D.,

El-Adawy, H., Melzer, F., Elschner, M., Neubauer, H. and Grace, D. 2016. Serological and

molecular investigation for brucellosis in swine in selected districts of Uganda. Tropical

Animal Health and Production 48(6): 1147–1155. http://dx.doi.org/10.1007/s11250-016-

1067-9

Stentiford, G.D., Becnel, J.J., Weiss, L.M., Keeling, P.J., Didier, E.S., Williams, B.A.P.,

Bjornson, S., Kent, M.L., Freeman, M.A., Brown, M.J.F., Troemel, E.R., Roesel, K.,

Sokolova, Y., Snowden, K.F. and Solter, L. 2016. Microsporidia – Emergent pathogens in

the global food chain. Trends in Parasitology 32(4): 336-348.

http://dx.doi.org/10.1016/j.pt.2015.12.004

Atherstone, C., Smith, E., Ochungo, P., Roesel, K. and Grace, D. 2017. Assessing the potential

role of pigs in the epidemiology of Ebola virus in Uganda. Transboundary and Emerging

Diseases. https://dx.doi.org/10.1111/tbed.12394 [Epub Aug 2015]

Dione, M.M., Akol, J., Roesel, K., Kungu, J., Ouma, E.A., Wieland, B. and Pezo, D. 2017.

Risk factors for African swine fever in smallholder pig production systems in Uganda.

Transboundary and Emerging Diseases 64(3):872-882.

https://dx.doi.org/10.1111/tbed.12452 [Epub Dec 2015]

112

http://www.ifrj.upm.edu.my/ifrj-2017-24-issue-4.html

http://dx.doi.org/10.1007/s00436-017-5450-x

http://dx.doi.org/10.1371/journal.pone.0166258

http://dx.doi.org/10.1007/s00436-016-5296-7

http://dx.doi.org/10.1007/s00436-016-5296-7

http://dx.doi.org/10.1017/S1466252316000104

http://dx.doi.org/10.1007/s11250-016-1067-9

http://dx.doi.org/10.1007/s11250-016-1067-9

http://dx.doi.org/10.1016/j.pt.2015.12.004

https://dx.doi.org/10.1111/tbed.12394

https://dx.doi.org/10.1111/tbed.12452

Publications

Dione, M.M., Ouma, E.A., Roesel, K., Kungu, J., Lule, P. and Pezo, D. 2014. Participatory


in three high poverty districts in Uganda. Preventive Veterinary Medicine 117(3-4):565-576.

https://dx.doi.org/10.1016/j.prevetmed.2014.10.012;

https://dx.doi.org/10.1016/j.prevetmed.2015.03.010

Under review at the time of graduation (shared first authorship):

Musewa, A., Roesel, K., Grace, D., Dione, M., Erume, J. Detection of Erysipelothrix

rhusiopathiae in naturally infected pigs in Kamuli district, Uganda.

Ndoboli, D., Roesel, K., Heilmann, M., Alter, T., Clausen, P.-H., Wampande, E., Grace, D.,

Huehn, S. Serotypes and antimicrobial resistance patterns of Salmonella enterica subsp.

enterica in pork and related fresh vegetable servings among pork outlets in Kampala,

Uganda.

2. Conference presentations

Roesel, K., Makita, K., Grace, D., 2017. Food safety research for development in sub-Saharan

Africa: Tapping the expertise of German partners. Poster presented at the Joint International

Symposium “Global Past, Present and Future Challenges in Risk Assessment –

Strengthening Consumer Health Protection” at the German Federal Institute for Risk

Assessment (BfR), Berlin, Germany, 29 November to 1 December 2017. Nairobi, Kenya:

ILRI.

Alonso, S., Roesel, K., Opiyo, S., Stomeo, F. and Grace, D. 2017. Metagenomics in food

safety: What's the added value? Case studies from the livestock sector in Tanzania and

Uganda. Presented at the FAO Regional Meeting on Agricultural Biotechnologies in

Sustainable Food Systems and Nutrition in sub-Saharan Africa, Addis Ababa, Ethiopia, 22–

24 November 2017. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/89560

Grace, D., Alonso, S., Dominguez-Salas, P., Fahrion, A., Häsler, B., Heilmann, M., Hoffmann,

V., Kang'ethe, E. and Roesel, K. 2017. Food safety metrics relevant to low- and middle-

income countries. Poster prepared for the 2nd annual Agriculture, Nutrition and Health

(ANH) Academy Week, Kathmandu, Nepal, 9–13 July 2017. Nairobi, Kenya: ILRI.


Roesel, K. 2017. Food safety interventions: economic and health outcomes and impacts.

Presentation at a Brussels Development Briefing on "Better targeting food safety

investments in low and middle income countries", Brussels, Belgium, 24 May 2017. Nairobi,

Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/82661

Roesel, K. 2016. Verbreitung des Hausschweins in Uganda: Chancen & Herausforderungen.

Presentation at 57. Conference of the food safety chapter of the German Veterinary

Association (DVG), 29 September 2016, Garmisch-Partenkirchen, Germany.


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Roesel, K., Schares, G., Grace, D., Baumann, M.P.O., Fries, R., Dione, M. and Clausen, P.-

H. 2016. The occurrence of porcine Toxoplasma gondii infections in smallholder production

systems in Uganda. Presentation at the first joint conference of the Association of Institutions

for Tropical Veterinary Medicine and the Society of Tropical Veterinary Medicine, Berlin,

Germany, 4–8 September 2016. Nairobi, Kenya: ILRI.


Ndoboli, D., Heilmann, M., Roesel, K., Clausen, P.-H., Wampande, E., Grace, D., Alter, T.

and Huehn, S. 2016. Antimicrobial resistance of Salmonella enterica in pork and vegetable

servings at pork joints in Kampala, Uganda. Poster presented at the first joint conference of

the Association of Institutions for Tropical Veterinary Medicine and the Society of Tropical

Veterinary Medicine, Berlin, Germany, 4–8 September 2016. Nairobi, Kenya: ILRI.


Heilmann, M., Roesel, K., Clausen, P.-H. and Grace, D. 2016. Knowledge, attitudes and

practices among customers at pork butcheries in Kampala, Uganda. Presentation at the first

joint conference of the Association of Institutions for Tropical Veterinary Medicine and the

Society of Tropical Veterinary Medicine, Berlin, Germany, 4–8 September 2016. Berlin,

Germany: Freie Universität Berlin. https://cgspace.cgiar.org/handle/10568/77090

Musewa, A., Roesel, K., Nakanjako, D., Grace, D., Ssenyonga, R., Nangendo, J., Kawooya, I.

and Erume, J. 2016. Erysipelothrix rhusiopathiae infection in pigs, pork and raw pork

handlers in Kamuli District, Eastern Uganda. Presentation at the first joint conference of the

Association of Institutions for Tropical Veterinary Medicine and the Society of Tropical

Veterinary Medicine, Berlin, Germany, 4–8 September 2016. Nairobi, Kenya: ILRI.


Hyera, E., Msalya, G., Karimuribo, E.D., Kurwijila, L.R., Alonso, S., Roesel, K. and Grace,

D. 2016. Isolation and identification of Listeria species along the milk value chain in one

region of Tanzania. Poster presented at the first joint conference of the Association of

Institutions for Tropical Veterinary Medicine and the Society of Tropical Veterinary

Medicine, Berlin, Germany, 4–8 September 2016. Kilimanjaro, Tanzania: Tanzania

Livestock Research Institute. https://cgspace.cgiar.org/handle/10568/77092

Alonso, S., Kang'ethe, E., Roesel, K., Dror, I. and Grace, D. 2015. 'You have an SMS’:

Innovative knowledge transfer for agriculture and health. Poster prepared for the European

College of Veterinary Public Health (ECVPH) annual scientific conference, Belgrade,

Serbia, 7-10 October 2015. Nairobi, Kenya: ILRI.


Roesel, K., Dione, M., Nöckler, K., Fries, R., Baumann, M.P.O., Clausen, P.-H. and Grace, D.

2015. Exposure of pigs to Trichinella spp. in three districts in Central and Eastern Uganda.

Abstract of paper presented at the 14th International Conference on Trichinellosis, Berlin,

Germany, 14-18 September 2015. https://cgspace.cgiar.org/handle/10568/68510

Heilmann, M., Mtimet, N., Roesel, K. and Grace, D. 2015. Assessing Ugandan pork butchers’

practices and their perception of customers’ preferences: A best-worst approach. Poster

prepared for the 9th European Congress on Tropical Medicine and International Health,

114

Publications








Publications

Basel, Switzerland, 6–10 September 2015. Nairobi, Kenya: ILRI.


Grace, D., Unger, F., Roesel, K., Tinega, G., Ndoboli, D., Sinh Dang-Xuan, Hung Nguyen-

Viet and Robinson, T. 2015. Present and future use of antimicrobials in pigs with case studies

from Uganda and Vietnam. Presented at the Safe Pork 2015 Conference, Porto, Portugal, 8-

10 September 2015. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/68304

Heilmann, M., Ndoboli, D., Roesel, K., Grace, D., Huehn, S., Bauer, B. and Clausen, P.-H.

2015. Occurrence of Salmonella spp. in flies and foodstuff from pork butcheries in Kampala,

Uganda. Presented at the Annual Expert Meeting on Parasitology and Parasitic Diseases at

the German Veterinary Association, Stralsund, Germany, 29 June–1 July 2015. Nairobi,


Roesel, K., Dione, M., Fries, R., Baumann, M.P.O., Nöckler, K., Schares, G., Grace, D. and

Clausen, P.-H. 2015. Assessment of the parasitic burden in smallholder pig value chains and

implications for public health in Uganda. Abstract of paper presented at the annual expert

meeting on parasitology and parasitic diseases at the German Veterinary Association,

Stralsund, Germany, 29 June – 1 July 2015. https://cgspace.cgiar.org/handle/10568/68301

Dione, M.M., Pezo, D.A., Ouma, E.A., Roesel, K., Brandes-van Dorresteijn, D. and Kawuma,

B. 2015. Training on management of endemic diseases for pig value chains in Uganda.

Presented at the 4th International Conference on Sustainable Livelihoods and Health in

Africa, Kampala, Uganda, 18-19 June 2015. Nairobi, Kenya: ILRI.


Alonso, S., Ocaido, M., Carron, M., Roesel, K. and Grace, D. 2015. Foodborne hazards in the

scientific literature: Results of a systematic literature review in East African countries.

Presented at the Regional Conference on Zoonotic Diseases in Eastern Africa, Naivasha,

Kenya, 9–12 March 2015. Nairobi, Kenya: ILRI.


Ouma, E., Roesel, K., Dione, M., Carter, N., Pezo, D., Ejobi, F. and Grace, D. 2014.

Participatory research for development to upgrade smallholder pig value chains in Uganda.

Poster presented at the Tropentag 2014 Conference on Bridging the Gap between Increasing

Knowledge and Decreasing Resources, Prague, Czech Republic, 17-19 September 2014.

Nairobi, Kenya. ILRI. https://cgspace.cgiar.org/handle/10568/43794

Pezo, D., Ouma, E. A., Lule, P., Dione, M., Lukuyu, B., Carter, N. and Roesel, K. 2014. The

feeding component in rural and peri-urban smallholder pig systems in Uganda. Poster

presented at the Tropentag 2014 Conference on Bridging the Gap between Increasing

Knowledge and Decreasing Resources, Prague, Czech Republic, 17-19 September 2014.

Nairobi, Kenya. ILRI. https://cgspace.cgiar.org/handle/10568/43793

Grace, D., Roesel, K., Bett, B. and Unger, F. 2014. Healthy lives: Tackling food-borne diseases

and zoonoses. Presented at the Tropentag 2014 Conference on Bridging the Gap between

Increasing Knowledge and Decreasing Resources, Prague, Czech Republic, 17-19

September 2014. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/44918

115










Makita, K., Roesel, K., Hung Nguyen-Viet, Bonfoh, B., Kang'ethe, E., Lapar, L. and Grace,

D. 2014. Food safety issues and scientific advances related to animal-source foods. Presented

at the Asia-Pacific Association of Agricultural Research Institutions (APAARI)-Japan

International Research Center for Agricultural Sciences (JIRCAS) expert consultation on

assuring food safety in Asia-Pacific, Tsukuba, Japan, 4-5 August 2014. Nairobi, Kenya:

ILRI. https://cgspace.cgiar.org/handle/10568/56885

Grace, D., Kang'ethe, E., Bonfoh, B., Roesel, K. and Makita, K. 2014. Food safety policy in 9

African countries. Presented at the 4th annual Leverhulme Centre for Integrative Research

on Agriculture and Health (LCIRAH) conference, London, UK, 3-4 June 2014. Nairobi,


Shija F, Nonga H, Kurwijila LR, Roesel K, Grace D and Misinzo G. 2013. Determination of

risk factors contributing to microbial contamination in milk and identification of presence of

selected pathogenic bacteria along dairy value chain in Tanga. Presentation at the 31st

Tanzania Veterinary Association scientific conference, Arusha, Tanzania, 3-5 December

2013. https://cgspace.cgiar.org/handle/10568/34880

Atherstone, C., Roesel, K. and Grace, D. 2013. Ebola risk in the pig value chain in Uganda.

Presented at the First African Regional Conference of the International Association on

Ecology and Health (Africa 2013 Ecohealth), Grand Bassam, Côte d'Ivoire, 1-5 October

2013. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/34388

Grace, D. and Roesel, K. 2013. Gender aspects of informal markets. Presented at the First

African Regional Conference of the International Association on Ecology and Health (Africa

2013 Ecohealth), Grand-Bassam, Côte d'Ivoire, 1-5 October 2013. Nairobi, Kenya: ILRI.


Roesel, K., Grace, D., Dione, M.M., Ouma, E.A., Pezo, D., Kungu, J., Ejobi, F. and Clausen,

P.H. 2013. Assessment of knowledge, attitudes and practices on pork safety among

smallholder pig farmers in Uganda. Poster prepared for the First African Regional

Conference of the International Association on Ecology and Health (Africa 2013 Ecohealth),

Grand-Bassam, Côte d'Ivoire, 1-5 October 2013. Nairobi, Kenya: ILRI.

https://cgspace.cgiar.org/handle/10568/33796 (Award for best poster)

Msalya, G., Joseph, E., Shija, F., Kurwijila, L.R., Grace, D., Roesel, K., Haesler, B., Ogutu,

F.,Fetsch, A., Misinzo, G. and Nonga, H. 2013. An integrated approach to assessing and

improving milk safety and nutrition in the Tanzanian dairy chain. Presentation at the First

African Regional Conference of the International Association on Ecology and Health (Africa

2013 Ecohealth), Grand-Bassam, Côte d'Ivoire, 1-5 October 2013. Morogoro, Tanzania:

Sokoine University of Agriculture. https://cgspace.cgiar.org/handle/10568/34867

Ocaido, M., Roesel, K. and Grace, D. 2013. Food safety and zoonotic hazards in pig value

chains in East Africa. Oral presentation at the First African Regional Conference of the

International Association on Ecology and Health (Africa 2013 Ecohealth), Grand-Bassam,

Côte d'Ivoire, 1-5 October 2013. Makerere, Uganda: Makerere University.


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Publications

Dewe, T., Roesel, K., Fekele, A., Legese, G. and Grace, D. 2013. An integrated approach to

assessing and improving meat and milk safety and nutrition in the Ethiopian sheep and goat

value chain. Presented at the First African Regional Conference of the International

Association on Ecology and Health (Africa 2013 Ecohealth), Grand-Bassam, Côte d'Ivoire,

1-5 October 2013. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/33805

Dione, M.M., Ouma, E.A., Roesel, K., Mayega, L., Nadiope, G., Kiryabwire, D. and Pezo, D.

2013. Participatory assessment of animal health constraints and husbandry practices in the

pig production system in three districts of Uganda. Poster prepared for the 14th International

Conference of the Association of Institutions for Tropical Veterinary Medicine (AITVM),

Johannesburg, South Africa, 25-29 August 2013. Nairobi, Kenya: ILRI.


Shija, F., Misinzo, G., Nonga, H., Kurwijila, L.R., Roesel, K. and Grace, D. 2013. The use of

polymerase chain reaction (PCR) to confirm presence of selected pathogenic bacteria along

milk value chain in Tanga region. Paper presented at the 14th international conference of the

Association of Institutions for Tropical Veterinary Medicine (AITVM), Johannesburg, South

Africa, 25-29 August 2013. https://cgspace.cgiar.org/handle/10568/33742

Roesel, K., Holmes, K., Kungu, J., Grace, D., Pezo, D.Q., Ouma, E.A., Baumann, M., Fries,

R., Ejobi, F. and Clausen, P.H. 2013. Fit for human consumption? A qualitative survey at a

Ugandan pig abattoir. Oral presentation at the 14th international conference of the

Association of Institutions for Tropical Veterinary Medicine (AITVM), Johannesburg, South

Africa, 25-29 August 2013. https://cgspace.cgiar.org/handle/10568/33725

Dewé, T.C.M., Roesel, K., Legese, G. and Grace, D. 2013. Lambs to the slaughter: Are meat

and milk from small ruminants a health risk to Ethiopians? Poster prepared for the 2013

annual conference of the Society for Veterinary Epidemiology and Preventive Medicine held

at Madrid, Spain, 20-22 March 2013. Nairobi, Kenya: ILRI.


3. Conference papers

Roesel, K. and Grace, D. 2015. Parasites in food chains. Presented at “Microsporidia in the

Animal to Human Food Chain: An International Symposium to Address Chronic Epizootic

Disease”, Vancouver, Canada, 9-13 August 2015. Nairobi, Kenya: ILRI.


Roesel, K., Grace, D., Baumann, M., Fries, R. and Clausen, P.-H. 2015. Food safety in low

income countries. Presented at the 15th expert conference on meat and poultry hygiene,

Berlin, Germany, 3-4 March 2015. Nairobi, Kenya: ILRI.


Roesel, K., Ouma, E.A., Dione, M.M., Pezo, D., Grace, D. and Alonso, S. 2014. Smallholder

pig producers and their pork consumption practices in three districts in Uganda. Presented

at the 6th All Africa Conference on Animal Agriculture, Nairobi, Kenya, 27-30 October


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4. Presentations at stakeholder workshops

Ouma, E., Dione, M., Roesel, K., Lule, P., Kawuma, B., Birungi, R., Asiimwe, G., Opio, F.

and Lukuyu, B. 2017. Smallholder pig value chains transformation in Uganda: Results,

lessons and insights. Presented at the Uganda Livestock Sector Consultative Meeting,

Kampala, 14 March 2017. Nairobi, Kenya: ILRI.


Roesel, K. 2017. Deutsche Veterinärmedizin in Sub-Sahara Afrika: Wo kann unser Beitrag

liegen? Beispiele aus der Praxis. Invited presentation at the Berlin Veterinary Association

(Berliner Tierärztliche Gesellschaft), Berlin, Germany, 12 April 2017. Nairobi, Kenya: ILRI.


Roesel, K. 2016. Nahrungsmittelsicherheit und informelle Märkte in Afrika südlich der

Sahara. Invited presentation at the GIZ expert colloquium, 20 July 2016, Bonn, Germany.


Roesel, K. 2015. The role of informal food markets: Towards professionalizing, not

criminalizing. Presented at the 16th Annual Meeting of the Inter-Agency Donor Group on

Pro-Poor Livestock Research and Development, Berlin, Germany, 18-20 November 2015.

Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/69118

Roesel, K. and Grace, D. 2015. Food safety and informal markets: Animal products in sub-

Saharan Africa. Presented at the monthly CGIAR Uganda Research Seminar, Kampala,

Uganda, 6 May 2015. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/66360

Roesel, K. and Tumwesige, V. 2014. From (bio)mass to (bio)gas - or, how to best utilize urban

slaughter waste. Presentation at an inception meeting of Wambizzi abattoir biogas study,

Kampala, Uganda, 24 September 2014. Nairobi, Kenya: ILRI.


Kasibule, D., Nsadha, Z. and Roesel, K. 2014. Value chain business models: The case of two

centralized slaughter slabs established in Kamuli. Presented at the Pre-evaluation workshop

of the ILRI Uganda Smallholder Pig Value Chain Development Project, Kampala. August


Roesel, K. 2014. Milk, meat and fish – More than just food: Current research on food safety

in sub-Saharan Africa. Presented at the University of Veterinary Medicine (Vetmeduni),

Vienna, Austria, 23 May 2014. Nairobi, Kenya: ILRI.


Roesel, K. and Ejobi, F. 2014. Safe Food Fair Food, Uganda: Rapid assessment report 2014.

Presented at the Safe Food, Fair Food Annual Project Planning Meeting, Addis Ababa,

Ethiopia, 15-17 April 2014. Nairobi, Kenya: ILRI.


Roesel, K., Clausen, P.H., Fries, R., Baumann, M., Noeckler, K. and Grace, D. 2013. More

pork and less parasites: A farm to fork approach for assessment and management of pork

meat associated diseases in Uganda. Presented at a parasitological colloquium, Berlin,

118

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Publications

Germany, 18 October 2013. Nairobi, Kenya: ILRI.


Ouma, E., Dione, M., Lule, P., Roesel, K., Mayega, L., Kiryabwire, D., Nadiope, G., Carter,

N. and Pezo, D. 2013. The Uganda pig value chain: Constraints and characteristics of actors.

Poster prepared for the CGIAR Research Program on Livestock and Fish Gender Working

Group Planning Workshop, Addis Ababa, Ethiopia, 14-18 October 2013. Nairobi, Kenya:


Dione, M., Ouma, E., Roesel, K. and Pezo, D. 2013. Strengthening pig value chains and

managing ASF risk in Uganda: Identifying best bet solutions. Presented at the closing

Workshop of the BecA‐ILRI‐CSIRO‐AusAID Project on Understanding ASF Epidemiology

as a basis for Control, Nairobi, Kenya, 2‐3 October 2013. Nairobi, Kenya: ILRI.


Ouma, E.A., Pezo, D., Dione, M., Roesel, K., Mayega, L., Kiryabwire, D., Nadiope, G. and

Lule, P. 2013. Assessing smallholder pig value chains in Uganda: Tools used at the farmers'

node. Poster presented at the Agrifood Chain Toolkit Conference on Livestock and Fish

Value Chains in East Africa, Kampala, Uganda, 9-11 September 2013. Nairobi, Kenya:


Roesel, K. and Carter, N. 2013. Safe Food, Fair Food in Uganda. Presented at the PigRisk

Project Outcome Mapping and in-depth Survey Workshop, Hanoi, Vietnam, 18 June 2013.

Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/34352

Roesel, K. 2013. Rapid integrated assessment of food safety and nutrition: Context. Presented

at the PigRisk Project Outcome Mapping and in-depth Survey Workshop, Hanoi, Vietnam,

18 June 2013. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/34350

Dione, M.M., Ouma, E.A., Roesel, K., Mayega, L., Nadiope, G., Kyriabwire, D. and Pezo, D.

2013. Participatory assessment of animal health constraints and husbandry practices in the

pig production system in three districts of Uganda. Poster prepared for the ILRI APM 2013,

Addis Ababa, 15-17 May 2013. Nairobi, Kenya: ILRI.


Roesel, K. and Ejobi, F. 2013. Safe Food, Fair Food: Reporting on the consumer end of the

pig value chain in Uganda. Presented at the Workshop on In-depth smallholder pig value

chain assessment and preliminary identification of best-bet interventions, Kampala, 9-11

April 2013. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/29035

Pezo, D., Ouma, E., Dione, M. and Roesel, K. 2013. The smallholder pig in-depth value chain

assessment in Uganda: How was it conducted? Presented at the Workshop on In-depth

smallholder pig value chain assessment and preliminary identification of best-bet

interventions, Kampala, 9-11 April 2013. Nairobi, Kenya: ILRI.


Rischkowsky, B., Dewe, T. and Roesel, K. 2013. Safe Food, Fair Food: Summary of findings

within lowland goat and sheep value chains in Ethiopia. Presented at the Multi-stakeholder

Workshop for Targeting Action Research on Lowland Sheep and Goat Value Chains in

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Ethiopia, Debre Zeit 1-2 April 2013. Addis Ababa: CGIAR Research Program on Livestock

and Fish. https://cgspace.cgiar.org/handle/10568/27841


within sheep value chains in the Atsbi and Abergelle districts of the Ethiopian Highlands.

Presented at the Multi-stakeholder Workshop for Targeting Action Research on Atsbi sheep

and Abergelle goat Value Chains in Tigray, Ethiopia, Mekelle, 19-20 March 2013. Addis

Ababa: CGIAR Research Program on Livestock and Fish.



within sheep value chains in the Ethiopian Highlands. Presented at the Multi-stakeholder

Workshop for Targeting Action Research on Small Ruminant Value Chains in Ethiopia,

Addis Ababa, 14th-15th March 2013. Addis Ababa: CGIAR Research Program on Livestock

and Fish. https://cgspace.cgiar.org/handle/10568/27854

Roesel, K. and Holmes, K. 2012. Preliminary Survey Findings on Slaughter Hygiene at

Wambizzi Abattoir Presented at Bioversity Kampala, Uganda, 16 August 2012. Nairobi,


Pezo, D. and Roesel, K. 2012. Smallholder pig value chain R4D projects in Uganda. Presented

at the workshop on Preliminary Survey Findings on Slaughter Hygiene at Wambizzi

Abattoir, Bioversity Kampala, Uganda, 16 August 2012. Nairobi, Kenya: ILRI.


Pezo D and Roesel K. 2012. Smallholder pig value chain development in Uganda. Presentation

at a stakeholders' meeting, Wakiso, Uganda, 13 June 2012. Nairobi, Kenya: ILRI.


5. Working papers/ research reports

Roesel, K., Holmes, K. and Grace, D. 2016. Fit for human consumption? A descriptive study

of Wambizzi pig abattoir, Kampala, Uganda. ILRI/A4NH Discussion Paper 1. Nairobi,


Grace, D., Roesel, K., Kang’ethe, E., Bonfoh, B. and Theis, S. 2015. Gender roles and food

safety in 20 informal livestock and fish value chains. IFPRI Discussion Paper 1489.

Washington, DC: International Food Policy Research Institute.


Ouma, E.A., Dione, M.M., Lule, P., Pezo, D., Marshall, K., Roesel, K., Mayega, L.,

Kiryabwire, D., Nadiope, G. and Jagwe, J. 2015. Smallholder pig value chain assessment in

Uganda: Results from producer focus group discussions and key informant interviews. ILRI

Project Report. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/68011

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Publications

Atherstone, C., Roesel, K. and Grace, D. 2014. Ebola risk assessment in the pig value chain in

Uganda. ILRI Research Report 34. Nairobi, Kenya: ILRI.


6. Books

Roesel, K. and Grace, D. (eds.) 2014. Food safety and informal markets: Animal products in

sub-Saharan Africa. London, UK: Routledge. https://cgspace.cgiar.org/handle/10568/42438

Roesel, K. and Grace, D. (eds.). 2016. Sécurité sanitaire des aliments et marchés informels:

les produits d’origine animale en Afrique Subsaharienne. Nairobi, Kenya: ILRI.


7. Book Chapters

Boqvist, S., Roesel, K. and Magnusson, U. 2014. Microbial food safety and zoonoses in urban

and peri-urban agriculture. IN: Magnusson, U. and Bergman, K.F. (eds), Urban and peri-

urban agriculture for food security in low-income countries – Challenges and knowledge

gaps. Uppsala, Sweden: Swedish University of Agricultural Sciences: 27-32.


8. Training presentations/ reports

ILRI. 2017. MoreMilk project: Laboratory training on milk hygiene and safety. Report of a

training course held from 29 May to 10 June 2017. Nairobi, Kenya: ILRI.


Nakatudde, P., Dione, M.M., Roesel, K., Kawuma, B., Brandes-van Dorresteijn, D. and Smith,

J. 2015. Parasite control in pigs: Uganda smallholder pig value chain capacity development

training manual. ILRI manual 13. Nairobi, Kenya: ILRI.


ILRI. 2014. Hands-on training on harvesting in the smallholder pig value chains in Uganda.

Report of a training course held at Kampala, Uganda, 7-11 April 2014. Nairobi, Kenya: ILRI.


Roesel K. 2014. Pig and pork zoonoses in Uganda. Presented at a training course for pig

farmers organized by Pig Production and Marketing Uganda Ltd., Matugga, Uganda, 15

February 2014. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/35008

ILRI. 2014. How to improve pig farming: A training workshop by Pig Production and

Marketing Uganda Limited. Report of a training course held at Matugga, Uganda, 14-15

February 2014. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/35046

121










ILRI. 2012. Training on tools for a rapid integrated assessment of food safety and nutrition.

Report of a training course held at Morogoro, Tanzania, 20-22 November 2012. Nairobi,


9. ILRI Research Briefs

Roesel, K., Hilali, M. El-Dine., Grace, D., Wieland, B., Rischkowsky, B. and Hail, A. 2017.

Better hygienic milking practices to improve goat milk quality. SmaRT Ethiopia intervention

factsheet 2. Addis Ababa: ICARDA. https://cgspace.cgiar.org/handle/10568/80964

Roesel, K., Grace, D., Wieland, B. and Rischkowsky, B. 2017. Better hygienic practices to

improve small ruminant meat quality. SmaRT Ethiopia intervention factsheet 1. Addis

Ababa: ICARDA. https://cgspace.cgiar.org/handle/10568/80966

Dione, M., Steinaa, L., Okoth, E., Roesel, K. and Wieland, B. 2016. Pig diseases in Uganda:

Impacts on pig production, human health and nutrition. Livestock and Fish Brief 24. Nairobi,


Gemeda, B., Desta, D., Roesel, K., Okoth, E., Secchini, F., Liljander, A. and Wieland, B. 2016.

Interventions and tools to improve small ruminant health in Ethiopia. Livestock and Fish

Brief 25. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/80138

Heilmann, M., Ndoboli, D. and Roesel, K. 2016. Pork joints: A mushrooming business in

Uganda with implications for public health. ILRI Research Brief 66. Nairobi, Kenya: ILRI.


Roesel, K., Ejobi, F. and Grace, D. 2015. Nutrition and health risks in smallholder pig value

chains in Uganda: Results of an assessment. ILRI Research Brief 48. Nairobi, Kenya: ILRI.


Grace, D., Roesel, K. and Lore, T. 2014. Food safety in informal markets in developing

countries: An overview. ILRI Research Brief 19. Nairobi, Kenya: ILRI.


Traoré, S., Fokou, G., Ndour, P., Yougbare, B., Koné, P., Daouda, D., Alonso, S., Roesel, K.,

Grace, D. and Bonfoh, B. 2014. Assessment of health risks in the small ruminants value

chain in Senegal. ILRI Research Brief 57. Nairobi, Kenya: ILRI.


Grace, D., Roesel, K. and Lore, T. 2014. Food safety in informal markets in developing

countries: Lessons from research by the International Livestock Research Institute. ILRI

Research Brief 20. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/42452

Grace, D., Roesel, K. and Lore, T. 2014. Poverty and gender aspects of food safety and

informal markets in sub-Saharan Africa. ILRI Research Brief 21. Nairobi, Kenya: ILRI.


122

Publications












Publications

Kang’ethe, E., Grace, D., Roesel, K., Hendrickx, S. and Makita, K. 2014. Safety of animal-

source foods in informal markets in the East African Community: Policy engagements. ILRI

Policy Brief 13. Nairobi, Kenya: ILRI. https://cgspace.cgiar.org/handle/10568/52350

123


Disclosure

Disclosure of own share in the body of the work

The share of the authors who were involved in the publications of this work is listed below

according to the following criteria:

1. Idea

2. Design of study and/or experiment

3. Test execution

4. Data analysis

5. Manuscript writing

6. Mobilisation of funding and other resources

Publication I

Dione, M. M., Ouma, E.A., Roesel, K., Kungu, J., Lule, P., Pezo, D. 2014. Participatory


in three high poverty districts in Uganda. Prev Vet Med. 2014 Dec 1;117(3-4):565-76. doi:

10.1016/j.prevetmed.2014.10.012. Erratum in: Prev Vet Med. 2015 May 1;119(3-4):239.

1. CRP L&F

2. Dione, Roesel, Grace, Ouma, Pezo

3. Dione, Roesel, Ouma, Pezo, Lule, Kungu

4. Dione

5. Dione, Roesel, Ouma, Pezo, Lule

6. Randolph, Grace

Publication II

Roesel, K., Dohoo, I., Baumann, M., Dione, M., Grace, D., Clausen, P.-H. 2017. Prevalence and

risk factors for gastrointestinal parasites in small-scale pig enterprises in Central and

Eastern Uganda. Parasitol Res. [2016 Oct 26; Epub ahead of print] 116: 335-345. doi:

10.1007/s00436-016-5296-7

1. Roesel, Baumann, Clausen

2. Roesel, Dione

3. Roesel

4. Roesel, Dohoo

5. Roesel, Dohoo, Baumann, Grace, Dione, Clausen

6. Randolph, Grace

124

Disclosure

Publication III

Roesel, K., Nöckler, K., Baumann, M.P.O., Fries, R., Dione, M.M., Clausen, P.-H., Grace, D.

2016. First Report of the Occurrence of Trichinella-Specific Antibodies in Domestic Pigs in

Cetral and Eastern Uganda. 2016 Nov 21; 11(11):e0166258. doi: 10.1371/journal.pone.0166258

1. Roesel, Clausen, Baumann, Fries, Nöckler

2. Roesel, Clausen, Baumann, Fries, Dione, Nöckler

3. Roesel, Nöckler

4. Roesel

5. Roesel, Nöckler, Clausen, Grace, Dione, Baumann, Fries

6. Grace, Randolph, Nöckler

Publication IV

Roesel, K., Schares, G., Grace, D., Baumann, M.P.O., Fries, R., Dione, M., Clausen, P.-H. 2016.

The occurrence of porcine Toxoplasma gondii infections in smallholder production systems

in Central and Eastern Uganda. In: Clausen, P.-H., Baumann, M., Nijhof, A. (eds), Tropical

Animal Diseases and Veterinary Public Health: Joining Forces to Meet Future Global Challenges.

First Joint ATIVM-STVM Conference, Berlin, Germany, 4-8 September 2016. Giessen, Germany:

Verlag der DVG Service GmbH. Page 22.

1. Roesel, Baumann, Nöckler, Fries, Clausen

2. Roesel, Schares, Clausen, Baumann, Fries, Dione

3. Roesel, Schares

4. Roesel, Dohoo

5. Roesel, Schares, Clausen, Baumann, Fries, Dione, Grace

6. Grace, Randolph, Schares

Publication V

Roesel, K., Ouma, E.A., Dione, M.M., Pezo, D., Grace, D. 2014. Smallholder pig producers and

their pork consumption practices in Kamuli, Masaka and Mukono districts in Uganda. In:

Africa’s Animal Agriculture: Macro-trends and future opportunities. 6th All African Conference

on Animal Agriculture, Nairobi, Kenya, 27-30 October 2014, pages 166-168.

1. Roesel, Grace

2. Roesel, Grace, Ouma, Dione, Pezo

3. Roesel

4. Roesel

5. Roesel, Grace, Dione, Pezo, Ouma

6. Randolph, Grace

125

Acknowledgements

Acknowledgements

First and foremost, I want to thank my supervisor at the International Livestock Research Institute

(ILRI), Dr Delia Grace, a role model for female junior scientists. She had the confidence in me

and my research topic but moreover, she had faith that I could handle the double burden of

coordinating and implementing a multi-country project in parallel to my research project. She

found just the right balance of giving me freedom and support to grow my skills and to grow as a

person, especially as a women in science.

I am deeply grateful for my academic supervisor, Professor Peter-Henning Clausen who has

known and supported me for the past ten years. We share the same passion for research that

benefits smallholder livestock producers in sub-Saharan Africa, and I very much hope to continue

working with him over the years to come.

I am also endowed to the other members of my mentoring committee: Dr Maximilian Baumann

who introduced me to ILRI in 2011 as well as to basic statistics, Professor Reinhard Fries who has

supported my study beyond his retirement and even during Christmas breaks, and PD Dr Karsten

Nöckler at the Federal Institute for Risk Assessment who is incredibly organized, efficient and

made me get to the point more than once. Though not on paper, I was blessed with two more

outstanding mentors who must not go unmentioned. I want to thank Dr Gereon Schares at the

Friedrich-Loeffler-Institute in Greifswald, Germany, who hosted me at his laboratory twice in

2013 and 2014, and despite his busy schedule trained me in a number of assays to diagnose T.

gondii, together with his lab technicians Andrea Bärwald and Mareen Sens. Secondly, I want to

thank Dr Ian Dohoo, a world leading veterinary epidemiologist at the University of Prince Edwards

Islands in Canada. It was during an ILRI-hosted epidemiology training in Kenya in 2015 that he

got hooked with pig parasites in the tropics and I believe he may not comprehend the extent of

support, both in statistics but also mentally, he gave to me during that last year of my work on the

thesis.

I am obliged to my colleagues at ILRI-Uganda who went with me through the challenges of

aligning two ILRI research programs in Uganda: Dr Emily Ouma, Dr Michel Dione, Dr Danilo

Pezo, Rachel Miwanda, Paul Basajja, and Peter Lule as well as Dr Thomas Randolph who has led

the CRP Livestock and Fish from its inception in 2012. There would be no results to present

without all the support I received in the field during data collection. I am therefore deeply grateful

for all my colleagues in the field: The district veterinary officers Dres Lawrence Mayega, Daniel

Kasibule and David Kiryabwire; the veterinary officers Edward Mawanda, Milly Nanyolo, and

Joseph Sserwadda as well as our data and sample collectors and local facilitators Joyce Akol, Janet

Bagonza, David Buguma, Moses Dhukusooka, Joseph Erume, Robert Isabirye, Fred Kabanda,

Ivan Kakeeto, Charles Kategere, Henry Kirya, Noah Kiwanuka, Godfrey Kizito, Joseph Kungu,

Eve Luvumu, Abel Lyundhu, Lawrence Mayanja, Noah Mayanja, John Matovu, Josephine

Mukasa, Irene Mutambo, Angella Musewa, Gideon Nadiope, Winnie Nairuba, Peter Ssenabulya,

Peter Wagabaza, and Joan Wotali. At the College of Veterinary Medicine, Animal Resources and

Biosecurity I want to thank Dickson Ndoboli, Maria Tumwebaze, Steven Kakooza, Dr Edward

Wampande, William Muyumbya, Wilfred Eneku, and Dr Francis Ejobi. At Wambizzi abattoir I

thank Simon Lubega, David Waalabyeki, and Jane Lwanira for the kind cooperation and

facilitation. In addition, I am grateful for the support given by Dr Anne Mayer-Scholl and Peter

Bahn at the Federal Institute for Risk Assessment in Berlin in planning and carrying out the sub-

activity on the occurrence of Trichinella spp. I also want to thank Emmanuel Muunda and Nicholas

126

Acknowledgements

Ngwili, research assistants at ILRI-Nairobi, for validating all the data entered from our surveys.

Finally, I am grateful to the Uganda Ministry of Agriculture, Animal Industry and Fisheries for

supporting research on smallholder pig value chains in Uganda for the benefit of resource-poor

livestock keepers, and especially Dr Noelima Nantima for her active provision of help throughout

the study. Behind the administrative scenes at ILRI, I want to thank Wacera Ndonga, Rosekellen

Njiru and Sarah Ndung’u for helping with finances and logistics, Grace Miceka at IT for her remote

support to keep my laptop well maintained and healthy (a vital aspect when working in the field

in a low-income country!), and Tezira Lore, ILRI communications officer for proofreading many

of my reports and papers. At Freie Universität Berlin, I want to thank Angela Daberkow,

coordinator of the PhD Biomedical Sciences program at Dahlem Research School, and her helper

Marie-Kamala Hecker for keeping track of all my outputs and achievements. At the Institute for

Parasitology and Tropical Veterinary Medicine, I want to thank Louise Le Bel, Antje Hoppenheit,

Katharina Seidl, and Peggy Hoffmann-Köhler for support during my stays in Berlin.

When working abroad it becomes challenging to maintain old friendships. But some are meant to

stay forever. In my case it is Anne, my dear gal pal, whom I know since sixth grade and who knows

the pains and gains of preparing a PhD thesis and supported me during mine. I also thank Albert,

my Dutch-African friend, who, during my first stay in Malawi in 2005, taught me so much about

African society, culture and politics and briefed me perfectly for my later career. And I want to

thank my friend Jana who always gave me a place to stay when I visited Berlin for course work or

mentoring meetings, and helped me not to forget the great cultural life in Europe. In Uganda I

made new friends who lived with me through good and bad times of the life after work, and I am

incredibly grateful for Ulrike and Jonas (with Elly) as well as Amrei and Oliver (with Schappi) for

you-know-what. I also thank Christine, Ibrahim, Benson and Jasper for all the daily amenities,

including taking me to the abattoir at four in the morning despite the rains and collecting my meat

samples from the butchers on Christmas Day!

I want to thank my parents, Ingrid and Holger, for giving me plenty of opportunities which I

believe I utilized to the fullest. And lastly I want to thank Hubertus, my love, for supporting me

throughout most parts of this project, and still growing strong with me.

The research was carried out with the financial support of the Federal Ministry for Economic

Cooperation and Development, Germany, and the CGIAR Research Program on Agriculture for

Nutrition and Health, led by the International Food Policy Research Institute through the „Safe

Food, Fair Food“ project and the CGIAR Research Program on Livestock & Fish, led by the

International Livestock Research Institute.

127

Statement of authorship

Statement of authorship

Except where reference is made in the text, this dissertation contains no material published

elsewhere or extracted in whole or in parts from a dissertation presented by myself towards another

degree or diploma. Nobody else’s work has been used without due acknowledgement in the main

text of the dissertation. This dissertation has not been submitted for an award of any other degree

or diploma in any tertiary institution.

Berlin, 30th November 2017 Kristina Rösel

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